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Annual Review of Animal Biosciences

Volume 10, 2022

Nonhuman Primates in Translational Research

Abstract

Nonhuman primates are critically important animal models in which to study complex human diseases, understand biological functions, and address the safety of new diagnostics and therapies proposed for human use. They have genetic, physiologic, immunologic, and developmental similarities when compared to humans and therefore provide important preclinical models of human health and disease. This review highlights select research areas that demonstrate the importance of nonhuman primates in translational research. These include pregnancy and developmental disorders, infectious diseases, gene therapy, somatic cell genome editing, and applications of in vivo imaging. The power of the immune system and our increasing understanding of the role it plays in acute and chronic illnesses are being leveraged to produce new treatments for a range of medical conditions. Given the importance of the human immune system in health and disease, detailed study of the immune system of nonhuman primates is essential to advance preclinical translational research. The need for nonhuman primates continues to remain a high priority, which has been acutely evident during the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) global pandemic. Nonhuman primates will continue to address key questions and provide predictive models to identify the safety and efficiency of new diagnostics and therapies for human use across the lifespan.

Keyword(s): developmental disorders, gene therapy, immune system, in vivo imaging, infectious diseases, preclinical models
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/content/journals/10.1146/annurev-animal-021419-083813
2022-02-15
2024-04-26
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Literature Cited

  1. 1. 
    Stouffer RL, Woodruff TK. 2017. Nonhuman primates: a vital model for basic and applied research on female reproduction, prenatal development, and women's health. ILAR J. 58:281–94
     [Google Scholar]
  2. 2. 
    Shetty G, Mitchell JM, Lam TNA, Phan TT, Zhang J et al. 2021. Postpubertal spermatogonial stem cell transplantation restores functional sperm production in rhesus monkeys irradiated before and after puberty. Andrology 9:51603–16
     [Google Scholar]
  3. 3. 
    Walker ML, Herndon JG. 2008. Menopause in nonhuman primates?. Biol. Reprod. 79:398–406
     [Google Scholar]
  4. 4. 
    Shideler SE, Gee NA, Chen J, Lasley BL 2001. Estrogen and progesterone metabolites and follicle-stimulating hormone in the aged macaque female. Biol. Reprod. 65:1718–25
     [Google Scholar]
  5. 5. 
    Tardif S, Carille A, Elmore D, Williams LE, Rice K 2012. Reproduction and breeding of nonhuman primates. Nonhuman Primates in Biomedical Research C Abee, K Mansfield, S Tardif, T Morris 197–249 Cambridge, MA: Academic. , 2nd ed..
     [Google Scholar]
  6. 6. 
    Ramsey EM, Houston ML, Harris JWS 1976. Interactions of the trophoblast and maternal tissues in three closely related primate species. Am. J. Obstet. Gynecol. 124:647–52
     [Google Scholar]
  7. 7. 
    Houston ML. 1969. The development of the baboon (Papio sp.) placenta during the fetal period of gestation. Am. J. Anat. 126:17–29
     [Google Scholar]
  8. 8. 
    Riesche L, Tardif SD, Ross CN, deMartelly VA, Ziegler T, Rutherford JN. 2018. The common marmoset monkey: avenues for exploring the prenatal, placental, and postnatal mechanisms in developmental programming of pediatric obesity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 314:R684–92
     [Google Scholar]
  9. 9. 
    Bianchi DW, Khosrotehrani K, Way SS, MacKenzie TC, Bajema I, O'Donoghue K. 2021. Forever connected: the lifelong biological consequences of fetomaternal and maternofetal microchimerism. . Clin. Chem. 67:351–62
     [Google Scholar]
  10. 10. 
    Bakkour S, Baker C, Tarantal AF, Wen L, Busch MP et al. 2014. Analysis of maternal microchimerism in rhesus monkeys (Macaca mulatta) using real-time quantitative PCR amplification of MHC polymorphisms. Chimerism 5:6–15
     [Google Scholar]
  11. 11. 
    Jimenez DF, Leapley AC, Lee CI, Ultsch MN, Tarantal AF. 2005. Fetal CD34+ cells in the maternal circulation and long-term microchimerism in rhesus macaques (Macaca mulatta). Transplantation 79:142–46
     [Google Scholar]
  12. 12. 
    Messaoudi I, Estep R, Robinson B, Wong SW 2011. Nonhuman primate models of human immunology. Antioxid. Redox Signal. 14:261–73
     [Google Scholar]
  13. 13. 
    Mestas J, Hughes CCW. 2004. Of mice and not men: differences between mouse and human immunology. J. Immunol. 172:2731–38
     [Google Scholar]
  14. 14. 
    Gibbons DL, Spencer J. 2011. Mouse and human intestinal immunity: same ballpark, different players; different rules, same score. Mucosal Immunol 4:148–57
     [Google Scholar]
  15. 15. 
    Batchelder CA, Lee CCI, Duru N, Baker C, Swainson L et al. 2014. Myeloid-lymphoid ontogeny in the rhesus monkey (Macaca mulatta). Anat. Rec. 297:1392–406
     [Google Scholar]
  16. 16. 
    Sartoretti J, Eberhardt CS. 2021. The potential role of nonhuman primate models to better comprehend early life immunity and maternal antibody transfer. Vaccines 9:306
     [Google Scholar]
  17. 17. 
    Semmes EC, Chen JL, Goswami R, Burt TD, Permar SR, Fouda GG. 2021. Understanding early-life adaptive immunity to guide interventions for pediatric health. Front. Immunol. 11:595297
     [Google Scholar]
  18. 18. 
    Zimmerman P, Jones CE. 2021. Factors that influence infant immunity and vaccine responses. Pediatr. Infect. Dis. J. 40:S40–46
     [Google Scholar]
  19. 19. 
    Watts AM, Stanley JR, Shearer MH, Hefty PS, Kennedy RC. 1999. Fetal immunization of baboons induces a fetal-specific antibody response. Nat. Med. 5:427–30
     [Google Scholar]
  20. 20. 
    Barry PA, Lockridge KM, Salamat S, Tinling SP, Yue Y et al. 2006. Nonhuman primate models of intrauterine cytomegalovirus infection. ILAR J 47:49–64
     [Google Scholar]
  21. 21. 
    Panganiban AT, Blair RV, Hattler JB, Bohannon DG, Bonaldo MC et al. 2020. A Zika virus primary isolate induces neuroinflammation, compromises the blood-brain barrier and upregulates CXCL12 in adult macaques. Brain Pathol 30:1017–27
     [Google Scholar]
  22. 22. 
    Raper J, Kovacs-Balint Z, Mavigner M, Gumber S, Burke MW et al. 2020. Long-term alterations in brain and behavior after postnatal Zika virus infection in infant macaques. Nat. Commun. 11:2534
     [Google Scholar]
  23. 23. 
    Jain VG, Kong F, Kallapur SG, Presicce P, Senthamaraikannnan P et al. 2020. IRAK1 is a critical mediator of inflammation-induced preterm birth. J. Immunol. 204:2651–60
     [Google Scholar]
  24. 24. 
    Coleman M, Armistead B, Orvis A, Quach P, Brokaw A et al. 2021. Hyaluronidase impairs neutrophil function and promotes group B Streptococcus invasion and preterm labor in nonhuman primates. mBio 12:e03115-20
     [Google Scholar]
  25. 25. 
    Napolitano LA, Grant RM, Deeks SG, Schmidt D, De Rosa SC et al. 2001. Increased production of IL-7 accompanies HIV-1–mediated T-cell depletion: implications for T-cell homeostasis. Nat. Med. 7:73–79
     [Google Scholar]
  26. 26. 
    Fagnoni FF, Vescovini R, Mazzola M, Bologna G, Nigro E et al. 1996. Expansion of cytotoxic CD8+ CD28− T cells in healthy ageing people, including centenarians. Immunology 88:501–7
     [Google Scholar]
  27. 27. 
    Fagnoni FF, Vescovini R, Passeri G, Bologna G, Pedrazzoni M et al. 2000. Shortage of circulating naive CD8+ T cells provides new insights on immunodeficiency in aging. Blood 95:2860–68
     [Google Scholar]
  28. 28. 
    Nociari MM, Telford W, Russo C. 1999. Postthymic development of CD28−CD8+ T cell subset: age-associated expansion and shift from memory to naive phenotype. J. Immunol. 162:3327–35
     [Google Scholar]
  29. 29. 
    Wikby A, Ferguson F, Forsey R, Thompson J, Strindhall J et al. 2005. An immune risk phenotype, cognitive impairment, and survival in very late life: impact of allostatic load in Swedish octogenarian and nonagenarian humans. J. Gerontol. A 60:556–65
     [Google Scholar]
  30. 30. 
    Zheng HY, Zhang MX, Pang W, Zheng YT 2014. Aged Chinese rhesus macaques suffer severe phenotypic T- and B-cell aging accompanied with sex differences. Exp. Gerontol. 55:113–19
     [Google Scholar]
  31. 31. 
    Messaoudi I, Ingram DK. 2012. Overview of aging research using nonhuman primate models. Age 34:1047–49
     [Google Scholar]
  32. 32. 
    Asquith M, Haberthur K, Brown M, Engelmann F, Murphy A et al. 2012. Age-dependent changes in innate immune phenotype and function in rhesus macaques (Macaca mulatta). Pathobiol. Aging Age Relat. Dis. 2:118052
     [Google Scholar]
  33. 33. 
    Cicin-Sain L, Sylvester AW, Hagen SI, Siess DC, Currier N et al. 2011. Cytomegalovirus-specific T cell immunity is maintained in immunosenescent rhesus macaques. J. Immunol. 187:1722–32
     [Google Scholar]
  34. 34. 
    Didier ES, Sugimoto C, Bowers LC, Khan IA, Kuroda MJ. 2012. Immune correlates of aging in outdoor-housed captive rhesus macaques (Macaca mulatta). Immun. Ageing 9:25
     [Google Scholar]
  35. 35. 
    Oxford KL, dela Pena-Ponce MGA, Jensen K, Eberhardt MK, Spinner A et al. 2015. The interplay between immune maturation, age, chronic viral infection and environment. Immun. Ageing 12:3
     [Google Scholar]
  36. 36. 
    Zingernagel RM, Doherty PC. 1997. The discovery of MHC restriction. Immunol. Today 18:14–17
     [Google Scholar]
  37. 37. 
    Shiina T, Ota M, Shimizu S, Katsuyama Y, Hashimoto N et al. 2006. Rapid evolution of major histocompatibility complex class I genes in primates generates new disease alleles in humans via hitchhiking diversity. Genetics 173:1555–70
     [Google Scholar]
  38. 38. 
    Ohtsuka M, Inoko H, Kulski JK, Yoshimura S. 2008. Major histocompatibility complex (Mhc) class Ib gene duplications, organization and expression patterns in mouse strain C57BL/6. BMC Genom. 9:178
     [Google Scholar]
  39. 39. 
    Dawkins R, Leelayuwat C, Gaudieri S, Tay G, Hui J et al. 1999. Genomics of the major histocompatibility complex: haplotypes, duplication, retroviruses and disease. Immunol. Rev. 167:275–304
     [Google Scholar]
  40. 40. 
    Corcoran MM, Phad GE, Vázquez Bernat N, Stahl-Hennig C, Sumida N et al. 2016. Production of individualized V gene databases reveals high levels of immunoglobulin genetic diversity. Nat. Commun. 7:13642
     [Google Scholar]
  41. 41. 
    Ramesh A, Darko S, Hua A, Overman G, Ransier A et al. 2017. Structure and diversity of the rhesus macaque immunoglobulin loci through multiple de novo genome assemblies. Front. Immunol. 8:1407
     [Google Scholar]
  42. 42. 
    Jardine J, Julien JP, Menis S, Ota T, Kalyuzhniy O et al. 2013. Rational HIV immunogen design to target specific germline B cell receptors. Science 340:711–16
     [Google Scholar]
  43. 43. 
    Pappas L, Foglierini M, Piccoli L, Kallewaard NL, Turrini F et al. 2014. Rapid development of broadly influenza neutralizing antibodies through redundant mutations. Nature 516:418–22
     [Google Scholar]
  44. 44. 
    Penkler M, Hanson M, Biesma R, Müller R. 2019. DOHaD in science and society: emergent opportunities and novel responsibilities. J. Dev. Orig. Health Dis. 10:268–73
     [Google Scholar]
  45. 45. 
    Hagberg H, Gressens P, Mallard C. 2012. Inflammation during fetal and neonatal life: implications for neurologic and neuropsychiatric disease in children and adults. Ann. Neurol. 71:444–57
     [Google Scholar]
  46. 46. 
    Lockett GA, Human J, Holloway JW. 2015. Does allergy begin in utero?. Pediatr. Allergy Immunol. 26:394–402
     [Google Scholar]
  47. 47. 
    Sureshchandra S, Marshall NE., Messaoudi I. 2019. Impact of pregravid obesity on maternal and fetal immunity: fertile grounds for reprogramming. J. Leukoc. Biol. 106:1035–50
     [Google Scholar]
  48. 48. 
    Tarantal AF, Berglund L. 2014. Obesity and lifespan health—importance of the fetal environment. Nutrients 6:1725–36
     [Google Scholar]
  49. 49. 
    Ganu RS, Harris RA, Collins K, Aagaard KM 2012. Early origins of adult disease: approaches for investigating the programmable epigenome in humans, nonhuman primates, and rodents. ILAR J 53:306–21
     [Google Scholar]
  50. 50. 
    Kim CJ, Romero R, Chaemsaithong P, Kim JS 2015. Chronic inflammation of the placenta: definition, classification, pathogenesis, and clinical significance. Am. J. Obstet. Gynecol. 213:S53–69
     [Google Scholar]
  51. 51. 
    Koga K, Mor G. 2010. Toll-like receptors at the maternal-fetal interface in normal pregnancy and pregnancy disorders. Am. J. Reprod. Immunol. 63:587–600
     [Google Scholar]
  52. 52. 
    Cowan MJ, Chou S-H, Tarantal AF 2001. Tolerance induction post in utero stem cell transplantation. Stem Cells from Cord Blood, In Utero Stem Cell Development, and Transplantation-Inclusive Gene Therapy W Holzgreve, M Lessl 145–96 Ernst Schering Res. Found. Workshop 33 Berlin: Springer-Verlag
     [Google Scholar]
  53. 53. 
    Lee CI, Fletcher M, Tarantal AF 2005. Effect of age on the frequency, cell cycle, and lineage maturation of rhesus monkey CD34+ and hematopoietic progenitor cells. Pediatr. Res. 58:315–22
     [Google Scholar]
  54. 54. 
    Lewis K, Yoshimoto M, Takebe T 2021. Fetal liver hematopoiesis: from development to delivery. Stem Cell Res. Ther. 12:139
     [Google Scholar]
  55. 55. 
    Batchelder CA, Keyser JL, Lee CCI, Tarantal AF. 2013. Characterization of growth, glomerular number, and tubular proteins in the developing rhesus monkey kidney. Anat. Rec. 296:1747–57
     [Google Scholar]
  56. 56. 
    Batchelder CA, Lee CCI, Martinez ML, Tarantal AF. 2010. Ontogeny of the kidney and renal developmental markers in the rhesus monkey (Macaca mulatta). Anat. Rec. 293:1971–83
     [Google Scholar]
  57. 57. 
    Tarantal AF, Han VKM, Cochrum KC, Mok A, daSilva M, Matsell DG. 2001. Fetal rhesus monkey model of obstructive renal dysplasia. Kidney Int 59:446–56
     [Google Scholar]
  58. 58. 
    Hiatt MJ, Ivanova L, Toran N, Tarantal AF, Matsell DG. 2010. Remodeling of the fetal collecting duct epithelium. Am. J. Pathol. 176:630–37
     [Google Scholar]
  59. 59. 
    Plopper CG, Hyde DM. 1992. Epithelial cells of the bronchiole. Comparative Biology of the Normal Lung RA Parent 85–92 Boca Raton, FL: CRC Press
     [Google Scholar]
  60. 60. 
    Miller LA, Royer CM, Pinkerton KE, Schelegle ES. 2017. Nonhuman primate models of respiratory disease: past, present, and future. ILAR J 58:269–80
     [Google Scholar]
  61. 61. 
    Bao EL, Chystsiakova A, Brahmajothi MV, Sunday ME, Pavlisko EN et al. 2016. Bronchopulmonary dysplasia impairs L-type amino acid transporter-1 expression in human and baboon lung. Pediatr. Pulmonol. 51:1048–56
     [Google Scholar]
  62. 62. 
    Reyes LF, Restrepo MI, Hinojosa CA, Soni NJ, Shenoy AT et al. 2016. A non-human primate model of severe pneumococcal pneumonia. PLOS ONE 11:e0166092
     [Google Scholar]
  63. 63. 
    Singh DK, Singh B, Ganatra SR, Gazi M, Cole J et al. 2021. Responses to acute infection with SARS-CoV-2 in the lungs of rhesus macaques, baboons and marmosets. Nat. Microbiol. 6:73–86
     [Google Scholar]
  64. 64. 
    Zimmerman LI, Papin JF, Warfel J, Wolf RF, Kosanke SD, Merkel TJ. 2018. Histopathology of Bordetella pertussis in the baboon model. Infect. Immun. 86:e00511-18
     [Google Scholar]
  65. 65. 
    Rakic P. 1988. Specification of cerebral cortical areas. Science 241:170–76
     [Google Scholar]
  66. 66. 
    Gerschwind DH, Rakic P. 2003. Cortical evolution: Judge the brain by its cover. Neuron 80:633–47
     [Google Scholar]
  67. 67. 
    Clowry G, Molnar Z, Rakic P. 2010. Renewed focus on the developing human neocortex. J. Anat. 217:276–88
     [Google Scholar]
  68. 68. 
    Hansen DV, Liu JH, Parker PR, Kriegstein AR 2010. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554–61
     [Google Scholar]
  69. 69. 
    Homman-Ludiye J, Bourne JA. 2017. The marmoset: an emerging model to unravel the evolution and development of the primate neocortex. Dev. Neurobiol. 77:263–67
     [Google Scholar]
  70. 70. 
    Salter MW, Stevens B. 2017. Microglia emerge as central players in brain disease. Nat. Med. 23:1018–27
     [Google Scholar]
  71. 71. 
    Barger N, Keiter J, Kreutz A, Krishnamurthy A, Weidenthaler C et al. 2019. Microglia: an intrinsic component of the proliferative zones in the fetal rhesus monkey (Macaca mulatta) cerebral cortex. Cereb. Cortex 29:2782–96
     [Google Scholar]
  72. 72. 
    Cunningham CL, Martínez-Cerdeño V, Noctor SC. 2013. Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 33:4216–33
     [Google Scholar]
  73. 73. 
    Wolf SA, Boddeke HW, Kettenmann H. 2017. Microglia in physiology and disease. Annu. Rev. Physiol. 79:619–43
     [Google Scholar]
  74. 74. 
    Bilbo SD, Block CL, Hanamsagar R, Tran PK 2018. Beyond infection—maternal immune activation by environmental factors, microglial development, and relevance for autism spectrum disorders. Exp. Neurol. 299:241–51
     [Google Scholar]
  75. 75. 
    Gurung S, Reuter N, Preno A, Dubaut J, Nadeau H et al. 2019. Zika virus infection at mid-gestation results in fetal cerebral cortical injury and fetal death in the olive baboon. PLOS Pathog. 15:e1007507
     [Google Scholar]
  76. 76. 
    Tarantal AF, Hartigan-O'Connor DJ, Penna E, Kreutz A, Martinez ML, Noctor SC 2021. Fetal rhesus monkey first trimester Zika virus infection impacts cortical development in the second and third trimesters. Cereb. Cortex 31:2309–21
     [Google Scholar]
  77. 77. 
    Page NF, Gandal MJ, Estes ML, Cameron S, Buth J et al. 2021. Alterations in retrotransposition, synaptic connectivity, and myelination implicated by transcriptomic changes following maternal immune activation in nonhuman primates. Biol. Psychiatry 89:896–910
     [Google Scholar]
  78. 78. 
    Bauman MD, Lesh TA, Rowland DJ, Schumann CM, Smucny J et al. 2019. Preliminary evidence of increased striatal dopamine in a nonhuman primate model of maternal immune activation. Transl. Psychiatry 9:135
     [Google Scholar]
  79. 79. 
    Joers V, Masilamoni G, Kempf D, Weiss AR, Rotterman TM et al. 2020. Microglia, inflammation and gut microbiota responses in a progressive monkey model of Parkinson's disease: a case series. Neurobiol. Dis. 144:105027
     [Google Scholar]
  80. 80. 
    Beckman D, Chakrabarty P, Ott S, Dao A, Zhou E et al. 2021. A novel tau-based rhesus model of Alzheimer's pathogenesis. Alzheimer's Dement. 17:933–45
     [Google Scholar]
  81. 81. 
    Howland D, Ellederova Z, Aronin N, Fernau D, Gallagher J et al. 2020. Large animal models of Huntington's disease: what we have learned and where we need to go next. J. Huntingt. Dis. 9:201–16
     [Google Scholar]
  82. 82. 
    Uccelli A, Giunti D, Capello E, Roccatagliata L, Mancardi GL 2003. EAE in the common marmoset Callithrix jacchus. Int. MS J. 10:6–12
     [Google Scholar]
  83. 83. 
    Mandell DT, Kristoff J, Gaufin T, Gautam R, Ma D et al. 2014. Pathogenic features associated with increased virulence upon simian immunodeficiency virus cross-species transmission from natural hosts. J. Virol. 88:6778–92
     [Google Scholar]
  84. 84. 
    Martins MA, Watkins DI. 2018. What is the predictive value of animal models for vaccine efficacy in humans? Rigorous simian immunodeficiency virus vaccine trials can be instructive. Cold Spring Harb. Perspect. Biol. 10:a029504
     [Google Scholar]
  85. 85. 
    Pandrea I, Apetrei C, Dufour J, Dillon N, Barbercheck J et al. 2006. Simian immunodeficiency virus SIVagm.sab infection of Caribbean African green monkeys: a new model for the study of SIV pathogenesis in natural hosts. J. Virol. 80:4858–67
     [Google Scholar]
  86. 86. 
    Thippeshappa R, Kimata JT, Kaushal D. 2020. Toward a macaque model of HIV-1 infection: roadblocks, progress, and future strategies. Front. Microbiol. 11:882
     [Google Scholar]
  87. 87. 
    Estes JD, Wong SW, Brenchley JM. 2018. Nonhuman primate models of human viral infections. Nat. Rev. Immunol. 18:390–404
     [Google Scholar]
  88. 88. 
    Heise C, Miller CJ, Lackner A, Dandekar S. 1994. Primary acute simian immunodeficiency virus infection of intestinal lymphoid tissue is associated with gastrointestinal dysfunction. J. Infect. Dis. 169:1116–20
     [Google Scholar]
  89. 89. 
    Katzenstein TL, Oliveri RS, Benfield T, Eugen-Olsen J, Nielsen C et al. 2002. Cell-associated HIV DNA measured early during infection has prognostic value independent of serum HIV RNA measured concomitantly. Scand. J. Infect. Dis. 34:529–33
     [Google Scholar]
  90. 90. 
    Delobel P, Sandres-Sauné K, Cazabat M, Pasquier C, Marchou B et al. 2005. R5 to X4 switch of the predominant HIV-1 population in cellular reservoirs during effective highly active antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 38:382–92
     [Google Scholar]
  91. 91. 
    Brühl H, Cihak J, Stangassinger M, Schlöndorff D, Mack MJ 2001. Depletion of CCR5-expressing cells with bispecific antibodies and chemokine toxins: a new strategy in the treatment of chronic inflammatory diseases and HIV. Immunology 166:2420–26
     [Google Scholar]
  92. 92. 
    Evans DT, Silvestri G. 2013. Nonhuman primate models in AIDS research. Curr. Opin. HIV AIDS 8:255–61
     [Google Scholar]
  93. 93. 
    Whitney JB, Hill AL, Sanisetty S, Penaloza-MacMaster P, Liu J et al. 2014. Rapid seeding of the viral reservoir prior to SIV viraemia in rhesus monkeys. Nature 512:74–77
     [Google Scholar]
  94. 94. 
    Borducchi EN, Liu J, Nkolola JP, Cadena AM, Yu WH et al. 2018. Antibody and TLR7 agonist delay viral rebound in SHIV-infected monkeys. Nature 563:360–64
     [Google Scholar]
  95. 95. 
    Okoye AA, Hansen SG, Vaidya M, Fukazawa Y, Park H et al. 2018. Early antiretroviral therapy limits SIV reservoir establishment to delay or prevent post-treatment viral rebound. Nat. Med. 24:1430–40
     [Google Scholar]
  96. 96. 
    Qiao L, Martelli CMT, Raja AI, Sanchez Clemente N, de Araùjo TVB et al. 2021. Epidemic preparedness: Prenatal Zika virus screening during the next epidemic. BMJ Glob. Health 6:e005332
     [Google Scholar]
  97. 97. 
    Abbink P, Larocca RA, De La, Barrera RA, Bricault CA, Moseley ET et al. 2016. Protective efficacy of multiple vaccine platforms against Zika virus challenge in rhesus monkeys. Science 353:1129–32
     [Google Scholar]
  98. 98. 
    Pardi N, Hogan MJ, Pelc RS, Muramatsu H, Andersen H et al. 2017. Zika virus protection by a single low-dose nucleoside-modified mRNA vaccination. Nature 543:248–51
     [Google Scholar]
  99. 99. 
    Larson HJ, Hartigan-Go K, de Figueiredo A. 2019. Vaccine confidence plummets in the Philippines following dengue vaccine scare: why it matters to pandemic preparedness. Hum. Vaccines Immunother. 15:625–27
     [Google Scholar]
  100. 100. 
    Gaudinski MR, Houser KV, Morabito KM, Hu Z, Yamshchikov G et al. 2018. Safety, tolerability, and immunogenicity of two Zika virus DNA vaccine candidates in healthy adults: randomised, open-label, phase 1 clinical trials. Lancet 391:552–62
     [Google Scholar]
  101. 101. 
    Modjarrad K, Lin L, George SL, Stephenson KE, Eckels KH et al. 2019. Preliminary aggregate safety and immunogenicity results from three trials of a purified inactivated Zika virus vaccine candidate: phase 1, randomised, double-blind, placebo-controlled clinical trials. Lancet 39:563–71
     [Google Scholar]
  102. 102. 
    Chang MC, Hild S, Grieder F 2021. Nonhuman primate models for SARS-CoV-2 research: Consider alternatives to macaques. Lab Anim 50:113–14
     [Google Scholar]
  103. 103. 
    Klasse PJ, Nixon DF, Moore JP. 2021. Immunogenicity of clinically relevant SARS-CoV-2 vaccines in nonhuman primates and humans. Sci. Adv. 7:eabe8065
     [Google Scholar]
  104. 104. 
    Aid M, Busman-Sahay K, Vidal SJ, Maliga Z, Bondoc S et al. 2020. Vascular disease and thrombosis in SARS-CoV-2-infected rhesus macaques. Cell 183:1354–66
     [Google Scholar]
  105. 105. 
    Yu J, Tostanoski LH, Peter L, Mercado NB, McMahan K et al. 2020. DNA vaccine protection against SARS-CoV-2 in rhesus macaques. Science 369:806–11
     [Google Scholar]
  106. 106. 
    Graham C, Seow J, Huettner I, Khan H, Kouphou N et al. 2021. Neutralization potency of monoclonal antibodies recognizing dominant and subdominant epitopes on SARS-CoV-2 Spike is impacted by the B.1.1.7 variant. Immunity 54:1276–89.e6
     [Google Scholar]
  107. 107. 
    Wang Z, Schmidt F, Weisblum Y, Muecksch F, Barnes CO et al. 2021. mRNA vaccine-elicited antibodies to SARS-CoV-2 and circulating variants. Nature 592:616–22
     [Google Scholar]
  108. 108. 
    Wu K, Choi A, Koch M, Ma L, Hill A et al. 2021. Preliminary analysis of safety and immunogenicity of a SARS-CoV-2 variant vaccine booster. medRxiv. https://doi.org/10.1101/2021.05.05.21256716
    [Crossref]
  109. 109. 
    McMahan K, Yu J, Mercado NB, Loos C, Tostanoski LH et al. 2021. Correlates of protection against SARS-CoV-2 in rhesus macaques. Nature 590:630–34
     [Google Scholar]
  110. 110. 
    Corbett KS, Nason MC, Flach B, Gagne M, O'Connell S et al. 2021. Immune correlates of protection by mRNA-1273 immunization against SARS-CoV-2 infection in nonhuman primates. Science 373:6561eabj0299
     [Google Scholar]
  111. 111. 
    Klasse PJ, Moore JP. 2020. Antibodies to SARS-CoV-2 and their potential for therapeutic passive immunization. eLife 9:e57877
     [Google Scholar]
  112. 112. 
    Crotty S. 2019. T follicular helper cell biology: a decade of discovery and diseases. Immunity 50:1132–48
     [Google Scholar]
  113. 113. 
    Grifoni A, Weiskopf D, Ramirez SI, Mateus J, Dan JM et al. 2020. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell 181:1489–501
     [Google Scholar]
  114. 114. 
    Wang YD, Sin WY, Xu GB, Yang HH, Wong TY et al. 2004. T-cell epitopes in severe acute respiratory syndrome (SARS) coronavirus spike protein elicit a specific T-cell immune response in patients who recover from SARS. J. Virol. 78:5612–18
     [Google Scholar]
  115. 115. 
    Zhao J, Zhao J, Mangalam AK, Channappanavar R, Fett C et al. 2016. Airway memory CD4+ T cells mediate protective immunity against emerging respiratory coronaviruses. Immunity 44:1379–91
     [Google Scholar]
  116. 116. 
    Shaan Lakshmanappa Y, Elizaldi SR, Roh JW, Schmidt BA, Carroll TD et al. 2021. SARS-CoV-2 induces robust germinal center CD4 T follicular helper cell responses in rhesus macaques. Nat. Commun. 12:541
     [Google Scholar]
  117. 117. 
    Chandrashekar A, Liu J, Martinot AJ, McMahan K, Mercado NB et al. 2020. SARS-CoV-2 infection protects against rechallenge in rhesus macaques. Science 369:812–17
     [Google Scholar]
  118. 118. 
    Radtke S, Adair JE, Giese MA, Chan YY, Norgaard ZK et al. 2017. A distinct hematopoietic stem cell population for rapid multilineage engraftment in nonhuman primates. Sci. Transl. Med. 9:eaan1145
     [Google Scholar]
  119. 119. 
    Tarantal AF, Giannoni F, Lee CCI, Wherley J, Sumiyoshi T et al. 2012. Non-myeloablative conditioning regimen to increase engraftment of gene-modified hematopoietic stem cells in young rhesus monkeys. Mol. Ther. 20:1033–45
     [Google Scholar]
  120. 120. 
    Uchida N, Nassehi T, Drysdale CM, Gamer J, Yapundich M et al. 2019. Busulfan combined with immunosuppression allows efficient engraftment of gene-modified cells in a rhesus macaque model. Mol. Ther. 27:1586–96
     [Google Scholar]
  121. 121. 
    Mendell JR, Al-Zaidy SA, Rodino-Klapac LR, Goodspeed K et al. 2021. Current clinical applications of in vivo gene therapy with AAVs. Mol. Ther. 29:464–88
     [Google Scholar]
  122. 122. 
    Wilson JM, Flotte TR. 2020. Moving forward after two deaths in a gene therapy trial of myotubular myopathy. Hum. Gene Ther. 31:695–96
     [Google Scholar]
  123. 123. 
    Flotte TR. 2020. Revisiting the “new” inflammatory toxicities of adeno-associated virus vectors. Hum. Gene Ther. 31:398–99
     [Google Scholar]
  124. 124. 
    Patel SR, Lundgren TS, Spencer HT, Doering CB. 2020. The immune response to the fVIII gene therapy in preclinical models. Front. Immunol. 11:494
     [Google Scholar]
  125. 125. 
    Gruntman AM, Gernoux G, Tang Q, Ye GJ, Knop DR et al. 2019. Bridging from intramuscular to limb perfusion delivery of rAAV: optimization in a non-human primate study. Mol. Ther. Methods Clin. Dev. 13:233–42
     [Google Scholar]
  126. 126. 
    Gushchina LV, Frair EC, Rohan N, Bradley AJ, Simmons TR et al. 2021. Lack of toxicity in nonhuman primates receiving clinically relevant doses of an AAV9.U7snRNA vector designed to induce DMD exon 2 skipping. Hum. Gene Ther. 32:882–94
     [Google Scholar]
  127. 127. 
    Corti M, Cleaver B, Clément N, Conlon TJ, Faris KJ et al. 2015. Evaluation of readministration of a recombinant adeno-associated vector expressing acid alpha-glucosidase in Pompe disease: preclinical to clinical planning. Hum. Gene Ther. Clin. Dev. 26:185–93
     [Google Scholar]
  128. 128. 
    Greig JA, Limberis MP, Bell P, Chen SJ, Calcedo R et al. 2017. Non-clinical study examining AAV8.TBG.hLDLR vector-associated toxicity in chow-fed wild-type and LDLR+/− rhesus macaques. Hum. Gene Ther. Clin. Dev. 28:39–50
     [Google Scholar]
  129. 129. 
    Galvan A, Petkau TL, Hill AM, Korecki AJ, Lu G et al. 2021. Intracerebroventricular administration of AAV9-PHP.B SYN1-EmGFP induces widespread transgene expression in the mouse and monkey central nervous system. Hum. Gene Ther. 32:599–615
     [Google Scholar]
  130. 130. 
    Hordeaux J, Buza EL, Dyer C, Goode T, Mitchell TW et al. 2020. Adeno-associated virus-induced dorsal root ganglion pathology. Hum. Gene Ther. 31:808–18
     [Google Scholar]
  131. 131. 
    Kiss S, Oresic Bender K, Grishanin RN, Hanna KM, Nieves JD et al. 2021. Long-term safety evaluation of continuous intraocular delivery of aflibercept by the intravitreal gene therapy candidate ADVM-022 in nonhuman primates. Transl. Vis. Sci. Technol. 10:34
     [Google Scholar]
  132. 132. 
    Rodriguez-Bocanegra E, Wozar F, Seitz IP, Reichel FFL, Ochakovski A et al. 2021. Longitudinal evaluation of hyper-reflective foci in the retina following subretinal delivery of adeno-associated virus in non-human primates. Transl. Vis. Sci. Technol. 10:15
     [Google Scholar]
  133. 133. 
    Weed L, Ammar MJ, Zhou S, Wei Z, Serrano LW et al. 2019. Safety of same-eye subretinal sequential readministration of AAV2-hRPE65v2 in non-human primates. Mol. Ther. Methods Clin. Dev. 15:133–48
     [Google Scholar]
  134. 134. 
    Wang L, Breton C, Warzecha CC, Bell P, Yan H et al. 2021. Long-term stable reduction of low-density lipoprotein in nonhuman primates following in vivo genome editing of PCSK9. Mol. Ther. 29:2019–29
     [Google Scholar]
  135. 135. 
    Wang L, Smith J, Breton C, Clark P, Zhang J et al. 2018. Meganuclease targeting of PCSK9 in macaque liver leads to stable reduction in serum cholesterol. Nat. Biotechnol. 36:717–25
     [Google Scholar]
  136. 136. 
    Musunuru K, Chadwick AC, Mizoguchi T, Garcia SP, DeNizio JE et al. 2021. In vivo CRISPR base editing of PCSK9 durably lowers cholesterol in primates. Nature 593:429–34
     [Google Scholar]
  137. 137. 
    Rothgangl T, Dennis MK, Lin PJC, Oka R, Witzigmann D et al. 2021. In vivo adenine base editing of PCSK9 in macaques reduces LDL cholesterol levels. Nat. Biotechnol. 39:949–57
     [Google Scholar]
  138. 138. 
    Uchida N, Li L, Nassehi T, Drysdale CM, Yapundich M et al. 2021. Preclinical evaluation for engraftment of CD34+ cells gene-edited at the sickle cell disease locus in xenograft mouse and non-human primate models. Cell Rep. Med. 2:100247
     [Google Scholar]
  139. 139. 
    Humbert O, Radtke S, Samuelson C, Carrillo RR, Perez AM et al. 2019. Therapeutically relevant engraftment of a CRISPR-Cas9-edited HSC-enriched population with HbF reactivation in nonhuman primates. Sci. Transl. Med. 11:eaaw3768
     [Google Scholar]
  140. 140. 
    Peterson CW, Wang J, Norman KK, Norgaard ZK, Humbert O et al. 2016. Long-term multilineage engraftment of autologous genome-edited hematopoietic stem cells in nonhuman primates. Blood 127:2416–26
     [Google Scholar]
  141. 141. 
    Saha K, Sontheimer EJ, Brooks PJ, Dwinell MR, Gersbach CA et al. 2021. The NIH Somatic Cell Genome Editing program. Nature 592:195–204
     [Google Scholar]
  142. 142. 
    Tarantal AF. 2005. Ultrasound imaging in rhesus (Macaca mulatta) and long-tailed (Macaca fascicularis) macaques: reproductive and research applications. The Laboratory Primate S Wolfe-Coote 317–51 Cambridge, MA: Academic
     [Google Scholar]
  143. 143. 
    Ludwig KD, Fain SB, Nguyen SM, Golos TG, Reeder SB et al. 2019. Perfusion of the placenta assessed using arterial spin labeling and ferumoxytol dynamic contrast enhanced magnetic resonance imaging in the rhesus macaque. Magn. Reson. Med. 81:1964–78
     [Google Scholar]
  144. 144. 
    Macdonald JA, Corrado PA, Nguyen SM, Johnson KM, Francois CJ et al. 2019. Uteroplacental and fetal 4D flow MRI in the pregnant rhesus macaque. J. Magn. Reson. Imaging 49:534–45
     [Google Scholar]
  145. 145. 
    Rossano S, Toyonaga T, Berg E, Lorence I, Fowles K et al. n.d. Imaging the fetal nonhuman primate brain with SV2A positron emission tomography (PET). Manuscript submitted
     [Google Scholar]
  146. 146. 
    Henrich TJ, Hsue PY, Van Brocklin H. 2019. Seeing is believing: nuclear imaging of HIV persistence. Front. Immunol. 10:2077
     [Google Scholar]
  147. 147. 
    Santangelo PJ, Rogers KA, Zurla C, Blanchard EL, Gumber S et al. 2015. Whole-body immunoPET reveals active SIV dynamics in viremic and antiretroviral therapy-treated macaques. Nat. Methods 12:427–32
     [Google Scholar]
  148. 148. 
    Santangelo PJ, Cicala C, Byrareddy SN, Ortiz KT, Little D et al. 2018. Early treatment of SIV+ macaques with an α4β7 mAb alters virus distribution and preserves CD4+ T cells in later stages of infection. Mucosal Immunol. 11:932–46
     [Google Scholar]
  149. 149. 
    Schreiber-Stainthorp W, Solomon J, Lee JH, Castro M, Shah S et al. 2021. Longitudinal in vivo imaging of acute neuropathology in a monkey model of Ebola virus infection. . Nat. Comm. 12:2855
     [Google Scholar]
  150. 150. 
    Hartman AL, Nambulli S, McMillan CM, White AG, Tilston-Lunel NL et al. 2020. SARS-CoV-2 infection of African green monkeys results in mild respiratory disease discernible by PET/CT imaging. PLOS Pathog 16:e1008903
     [Google Scholar]
  151. 151. 
    Finch CL, Crozier I, Lee JH, Byrum R, Cooper TK et al. 2020. Characteristic and quantifiable COVID-19-like abnormalities in CT- and PET/CT-imaged lungs of SARS-CoV-2-infected crab-eating macaques (Macaca fascicularis). bioRxiv 096727. https://doi.org/10.1101/2020.05.14.096727
    [Crossref]
  152. 152. 
    Mattila JT, Beaino W, Maiello P, Coleman MT, White AG et al. 2017. Positron emission tomography imaging of macaques with tuberculosis identifies temporal changes in granuloma glucose metabolism and integrin α4β1-expressing immune cells. J. Immunol. 199:806–15
     [Google Scholar]
  153. 153. 
    Lindsay KE, Bhosle SM, Zurla C, Beyersdorf J, Rogers KA et al. 2019. Visualization of early events in mRNA vaccine delivery in non-human primates via PET-CT and near-infrared imaging. Nat. Biomed. Eng. 3:371–80
     [Google Scholar]
  154. 154. 
    Tarantal AF, Lee CCI, Jimenez DF, Cherry SR. 2006. Fetal gene transfer using lentiviral vectors: in vivo detection of gene expression by microPET and optical imaging in fetal and infant monkeys. Hum. Gene Ther. 12:1254–61
     [Google Scholar]
  155. 155. 
    Tarantal AF, Skarlatos SI. 2012. Center for Fetal Monkey Gene Transfer for Heart, Lung, and Blood Diseases: an NHLBI resource for the gene therapy community. Hum. Gene Ther. 23:1130–35
     [Google Scholar]
  156. 156. 
    Tarantal AF, Lee CCI. 2010. Long-term luciferase expression monitored by bioluminescence imaging after adeno-associated virus-mediated fetal gene delivery in rhesus monkeys (Macaca mulatta). Hum. Gene Ther. 21:143–48
     [Google Scholar]
  157. 157. 
    Huang J, Lee CCI, Sutcliffe JL, Cherry SR, Tarantal AF 2008. Radiolabeling monkey CD34+ hematopoietic and mesenchymal stem cells with 64Cu-PTSM for microPET. Mol. Imaging 7:1–11
     [Google Scholar]
  158. 158. 
    Tarantal AF, Lee CCI, Kukis D, Cherry SR 2013. Radiolabeling to monitor cell trafficking and engraftment of human peripheral blood stem cells by PET in young rhesus monkeys. PLOS ONE 8:e77148
     [Google Scholar]
  159. 159. 
    Tarantal AF, Lee CCI, Batchelder CA, Christensen JE, Prater D et al. 2012. Radiolabeling and in vivo imaging of transplanted renal lineages differentiated from human embryonic stem cells in fetal monkeys. Mol. Imaging Biol. 14:197–204
     [Google Scholar]
  160. 160. 
    Ballon DJ, Rosenberg JB, Fung EK, Nikolopoulou A, Kothari P et al. 2020. Quantitative whole-body imaging of I-124-labeled adeno-associated viral vector biodistribution in nonhuman primates. Hum. Gene Ther. 31:1237–59
     [Google Scholar]
  161. 161. 
    Stringaris K, Hoyt RF, Davidson-Moncada JK, Pantin JM, Tisdale JF et al. 2020. Intrabone transplantation of CD34+ cells with optimized delivery does not enhance engraftment in a rhesus macaque model. Blood Adv. 4:6148–56
     [Google Scholar]
  162. 162. 
    Sato N, Stringaris K, Davidson-Moncada JK, Reger R, Adler SS et al. 2020. In vivo tracking of adoptively transferred natural killer cells in rhesus macaques using 89zirconium-oxine cell labeling and PET imaging. Clin. Cancer Res. 26:2573–81
     [Google Scholar]
  163. 163. 
    Berg E, Gill H, Marik J, Ogasawara A, Williams S et al. 2020. Total-body PET and highly stable chelators together enable meaningful 89Zr-antibody PET studies up to 30 days after injection. J. Nucl. Med. 61:453–60
     [Google Scholar]
  164. 164. 
    Mattison JA, Vaughn KL. 2016. An overview of nonhuman primates in aging research. Exp. Gerontol. 94:41–45
     [Google Scholar]
  165. 165. 
    Souder DC, Dreischmeier IA, Smith AB, Wright S, Martin SA et al. 2021. Rhesus monkeys as a translational model for late-onset Alzheimer's disease. Aging Cell 5:e13374
     [Google Scholar]
  166. 166. 
    Ballanger B, Beaudoin-Gobert M, Neumane S, Epinat J, Metereau E et al. 2016. Imaging dopamine and serotonin systems on MPTP monkeys: a longitudinal PET investigation of compensatory mechanisms. J. Neurosci. 36:1577–89
     [Google Scholar]
  167. 167. 
    Tao Y, Vermilyea SC, Zammit M, Lu J, Olsen M, Metzger JM. 2021. Autologous transplant therapy alleviates motor and depressive behaviors in parkinsonian monkeys. Nat. Med. 27:632–39
     [Google Scholar]
  168. 168. 
    Shrestha S, Kim MJ, Eldridge M, Lehmann ML, Frankland M et al. 2020. PET measurement of cyclooxygenase-2 using a novel radioligand: upregulation in primate neuroinflammation and first-in-human study. J. Neuroinflamm. 17:140
     [Google Scholar]
  169. 169. 
    Hewitt JA, Lutz C, Florence WC, Pitt MLM, Rao S et al. 2020. ACTIVating resources for the COVID-19 pandemic: in vivo models for vaccines and therapeutics. Cell Host Microbe 28:646–59
     [Google Scholar]
  170. 170. 
    Hild SA, Chang MC, Murphy SJ, Greider FB 2021. Nonhuman primate models for SARS-CoV-2 research: infrastructure needs for pandemic preparedness. Lab Anim. 50:140–41
     [Google Scholar]
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