1932

Abstract

The peripheral nervous system (PNS) endows animals with the remarkable ability to sense and respond to a dynamic world. Emerging evidence shows the PNS also participates in tissue homeostasis and repair by integrating local changes with organismal and environmental changes. Here, we provide an in-depth summary of findings delineating the diverse roles of peripheral nerves in modulating stem cell behaviors and immune responses under steady-state conditions and in response to injury and duress, with a specific focus on the skin and the hematopoietic system. These examples showcase how elucidating neuro–stem cell and neuro–immune cell interactions provides a conceptual framework that connects tissue biology and local immunity with systemic bodily changes to meet varying demands. They also demonstrate how changes in these interactions can manifest in stress, aging, cancer, and inflammation, as well as how these findings can be harnessed to guide the development of new therapeutics.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-120320-032429
2022-10-06
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/38/1/annurev-cellbio-120320-032429.html?itemId=/content/journals/10.1146/annurev-cellbio-120320-032429&mimeType=html&fmt=ahah

Literature Cited

  1. Abraira VE, Ginty DD. 2013. The sensory neurons of touch. Neuron 79:618–39
    [Google Scholar]
  2. Adams SC, Schondorf R, Benoit J, Kilgour RD. 2015. Impact of cancer and chemotherapy on autonomic nervous system function and cardiovascular reactivity in young adults with cancer: a case-controlled feasibility study. BMC Cancer 15:414
    [Google Scholar]
  3. Akinrodoye MA, Lui F. 2022. Neuroanatomy, somatic nervous system. StatPearls Treasure Island, FL: StatPearls Publ.
    [Google Scholar]
  4. Alexander GM, Rogan SC, Abbas AI, Armbruster BN, Pei Y et al. 2009. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63:27–39
    [Google Scholar]
  5. Argyriou AA, Bruna J, Marmiroli P, Cavaletti G. 2012. Chemotherapy-induced peripheral neurotoxicity (CIPN): an update. Crit. Rev. Oncol. Hematol. 82:51–77
    [Google Scholar]
  6. Armbruster BN, Li X, Pausch MH, Herlitze S, Roth BL. 2007. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. PNAS 104:5163–68
    [Google Scholar]
  7. Armstrong AW, Mehta MD, Schupp CW, Gondo GC, Bell SJ, Griffiths CEM. 2021. Psoriasis prevalence in adults in the United States. JAMA Dermatol. 157:940–46
    [Google Scholar]
  8. Bajayo A, Bar A, Denes A, Bachar M, Kram V et al. 2012. Skeletal parasympathetic innervation communicates central IL-1 signals regulating bone mass accrual. PNAS 109:15455–60
    [Google Scholar]
  9. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M et al. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449:1003–7
    [Google Scholar]
  10. Baryawno N, Przybylski D, Kowalczyk MS, Kfoury Y, Severe N et al. 2019. A cellular taxonomy of the bone marrow stroma in homeostasis and leukemia. Cell 177:1915–32.e16
    [Google Scholar]
  11. Basbaum AI, Bautista DM, Scherrer G, Julius D 2009. Cellular and molecular mechanisms of pain. Cell 139:267–84
    [Google Scholar]
  12. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI et al. 2007. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204–8
    [Google Scholar]
  13. Beronja S, Livshits G, Williams S, Fuchs E. 2010. Rapid functional dissection of genetic networks via tissue-specific transduction and RNAi in mouse embryos. Nat. Med. 16:821–27
    [Google Scholar]
  14. Biaggioni I. 2008. Circadian clocks, autonomic rhythms, and blood pressure dipping. Hypertension 52:797–98
    [Google Scholar]
  15. Biemesderfer D, Munger BL, Binck J, Dubner R. 1978. The pilo-Ruffini complex: a non-sinus hair and associated slowly-adapting mechanoreceptor in primate facial skin. Brain Res. 142:197–222
    [Google Scholar]
  16. Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI et al. 2000. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405:458–62
    [Google Scholar]
  17. Botchkarev VA, Peters EM, Botchkareva NV, Maurer M, Paus R. 1999. Hair cycle-dependent changes in adrenergic skin innervation, and hair growth modulation by adrenergic drugs. J. Invest. Dermatol. 113:878–87
    [Google Scholar]
  18. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8:1263–68
    [Google Scholar]
  19. Brady RD, Wong KR, Robinson DL, Mychasiuk R, McDonald SJ et al. 2019. Bone health in rats with temporal lobe epilepsy in the absence of anti-epileptic drugs. Front. Pharmacol. 10:1278
    [Google Scholar]
  20. Braz JM, Nassar MA, Wood JN, Basbaum AI. 2005. Parallel “pain” pathways arise from subpopulations of primary afferent nociceptor. Neuron 47:787–93
    [Google Scholar]
  21. Brown HE, Dougherty TF. 1956. The diurnal variation of blood leucocytes in normal and adrenalectomized mice. Endocrinology 58:365–75
    [Google Scholar]
  22. Brownell I, Guevara E, Bai CB, Loomis CA, Joyner AL. 2011. Nerve-derived Sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 8:552–65
    [Google Scholar]
  23. Cavanaugh DJ, Chesler AT, Jackson AC, Sigal YM, Yamanaka H et al. 2011. Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J. Neurosci. 31:5067–77
    [Google Scholar]
  24. Chan KY, Jang MJ, Yoo BB, Greenbaum A, Ravi N et al. 2017. Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems. Nat. Neurosci. 20:1172–79
    [Google Scholar]
  25. Chang CY, Pasolli HA, Giannopoulou EG, Guasch G, Gronostajski RM et al. 2013. NFIB is a governor of epithelial-melanocyte stem cell behaviour in a shared niche. Nature 495:98–102
    [Google Scholar]
  26. Chen C-S, Barnoud C, Scheiermann C. 2021. Peripheral neurotransmitters in the immune system. Curr. Opin. Physiol. 19:73–79
    [Google Scholar]
  27. Chiu IM, Barrett LB, Williams EK, Strochlic DE, Lee S et al. 2014. Transcriptional profiling at whole population and single cell levels reveals somatosensory neuron molecular diversity. eLife 3:e04660
    [Google Scholar]
  28. Chiu IM, Heesters BA, Ghasemlou N, Von Hehn CA, Zhao F et al. 2013. Bacteria activate sensory neurons that modulate pain and inflammation. Nature 501:52–57
    [Google Scholar]
  29. Choi S, Zhang B, Ma S, Gonzalez-Celeiro M, Stein D et al. 2021. Corticosterone inhibits GAS6 to govern hair follicle stem-cell quiescence. Nature 592:428–32
    [Google Scholar]
  30. Chu C, Artis D, Chiu IM. 2020. Neuro-immune interactions in the tissues. Immunity 52:464–74
    [Google Scholar]
  31. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Förster I. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8:265–77
    [Google Scholar]
  32. Cohen JA, Edwards TN, Liu AW, Hirai T, Jones MR et al. 2019. Cutaneous TRPV1+ neurons trigger protective innate type 17 anticipatory immunity. Cell 178:919–32.e14
    [Google Scholar]
  33. De Giorgi V, Grazzini M, Benemei S, Marchionni N, Botteri E et al. 2018. Propranolol for off-label treatment of patients with melanoma: results from a cohort study. JAMA Oncol. 4:e172908–e08
    [Google Scholar]
  34. de Jonge WJ, van der Zanden EP, The FO, Bijlsma MF, van Westerloo DJ et al. 2005. Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway. Nat. Immunol. 6:844–51
    [Google Scholar]
  35. Dhaka A, Earley TJ, Watson J, Patapoutian A. 2008. Visualizing cold spots: TRPM8-expressing sensory neurons and their projections. J. Neurosci. 28:566–75
    [Google Scholar]
  36. Dong X, Han S, Zylka MJ, Simon MI, Anderson DJ. 2001. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 106:619–32
    [Google Scholar]
  37. Elefteriou F, Ahn JD, Takeda S, Starbuck M, Yang X et al. 2005. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 434:514–20
    [Google Scholar]
  38. English KB, Kavka-Van Norman D, Horch K. 1983. Effects of chronic denervation in type I cutaneous mechanoreceptors (Haarscheiben). Anat. Rec. 207:79–88
    [Google Scholar]
  39. Fan SM-Y, Chang Y-T, Chen C-L, Wang W-H, Pan M-K et al. 2018. External light activates hair follicle stem cells through eyes via an ipRGC–SCN–sympathetic neural pathway. PNAS 115:E6880–89
    [Google Scholar]
  40. Farber EM, Lanigan SW, Boer J. 1990. The role of cutaneous sensory nerves in the maintenance of psoriasis. Int. J. Dermatol. 29:418–20
    [Google Scholar]
  41. Farrell MS, Pei Y, Wan Y, Yadav PN, Daigle TL et al. 2013. A Gαs DREADD mouse for selective modulation of cAMP production in striatopallidal neurons. Neuropsychopharmacology 38:854–62
    [Google Scholar]
  42. Ferron M, Vacher J. 2005. Targeted expression of Cre recombinase in macrophages and osteoclasts in transgenic mice. Genesis 41:138–45
    [Google Scholar]
  43. Fujiwara H, Ferreira M, Donati G, Marciano DK, Linton JM et al. 2011. The basement membrane of hair follicle stem cells is a muscle cell niche. Cell 144:577–89
    [Google Scholar]
  44. Furlan A, La Manno G, Lübke M, Häring M, Abdo H et al. 2016. Visceral motor neuron diversity delineates a cellular basis for nipple- and pilo-erection muscle control. Nat. Neurosci. 19:1331–40
    [Google Scholar]
  45. Gabanyi I, Muller PA, Feighery L, Oliveira TY, Costa-Pinto FA, Mucida D. 2016. Neuro-immune interactions drive tissue programming in intestinal macrophages. Cell 164:378–91
    [Google Scholar]
  46. Gao X, Zhang D, Xu C, Li H, Caron KM, Frenette PS. 2021. Nociceptive nerves regulate haematopoietic stem cell mobilization. Nature 589:591–96
    [Google Scholar]
  47. García A, Arranz L, Sánchez-Aguilera A, Airaksinen M, Méndez-Ferrer S. 2013. Circadian parasympathetic regulation of hematopoietic stem cell traffic. Exp. Hematol. 41:S14
    [Google Scholar]
  48. García-García A, Korn C, García-Fernández M, Domingues O, Villadiego J et al. 2019. Dual cholinergic signals regulate daily migration of hematopoietic stem cells and leukocytes. Blood 133:224–36
    [Google Scholar]
  49. Ge Y, Miao Y, Gur-Cohen S, Gomez N, Yang H et al. 2020. The aging skin microenvironment dictates stem cell behavior. PNAS 117:5339–50
    [Google Scholar]
  50. Glasner A, Avraham R, Rosenne E, Benish M, Zmora O et al. 2010. Improving survival rates in two models of spontaneous postoperative metastasis in mice by combined administration of a β-adrenergic antagonist and a cyclooxygenase-2 inhibitor. J. Immunol. 184:2449–57
    [Google Scholar]
  51. Godinho-Silva C, Cardoso F, Veiga-Fernandes H. 2019. Neuro-immune cell units: a new paradigm in physiology. Annu. Rev. Immunol. 37:19–46
    [Google Scholar]
  52. Grover A, Sanjuan-Pla A, Thongjuea S, Carrelha J, Giustacchini A et al. 2016. Single-cell RNA sequencing reveals molecular and functional platelet bias of aged haematopoietic stem cells. Nat. Commun. 7:11075
    [Google Scholar]
  53. Haas S, Trumpp A, Milsom MD. 2018. Causes and consequences of hematopoietic stem cell heterogeneity. Cell Stem Cell 22:627–38
    [Google Scholar]
  54. Halberg F, Visscher MB, Bittner JJ. 1953. Eosinophil rhythm in mice: range of occurrence; effects of illumination, feeding, and adrenalectomy. Am. J. Physiol. 174:109–22
    [Google Scholar]
  55. Han L, Ma C, Liu Q, Weng H-J, Cui Y et al. 2013. A subpopulation of nociceptors specifically linked to itch. Nat. Neurosci. 16:174–82
    [Google Scholar]
  56. Hayakawa Y, Sakitani K, Konishi M, Asfaha S, Niikura R et al. 2017. Nerve growth factor promotes gastric tumorigenesis through aberrant cholinergic signaling. Cancer Cell 31:21–34
    [Google Scholar]
  57. Heidt T, Sager HB, Courties G, Dutta P, Iwamoto Y et al. 2014. Chronic variable stress activates hematopoietic stem cells. Nat. Med. 20:754–58
    [Google Scholar]
  58. Hjerling-Leffler J, Alqatari M, Ernfors P, Koltzenburg M. 2007. Emergence of functional sensory subtypes as defined by transient receptor potential channel expression. J. Neurosci. 27:2435–43
    [Google Scholar]
  59. Hoeffel G, Debroas G, Roger A, Rossignol R, Gouilly J et al. 2021. Sensory neuron-derived TAFA4 promotes macrophage tissue repair functions. Nature 594:94–99
    [Google Scholar]
  60. Hsu Y-C, Fuchs E. 2021. Building and maintaining the skin. Cold Spring Harb. Perspect. Biol. 14:a040840 https://cshperspectives.cshlp.org/content/14/7/a040840.short
    [Google Scholar]
  61. Huang S, Kuri P, Aubert Y, Brewster M, Li N et al. 2021a. Lgr6 marks epidermal stem cells with a nerve-dependent role in wound re-epithelialization. Cell Stem Cell 28:1582–96.e6
    [Google Scholar]
  62. Huang S, Ziegler CGK, Austin J, Mannoun N, Vukovic M et al. 2021b. Lymph nodes are innervated by a unique population of sensory neurons with immunomodulatory potential. Cell 184:441–59.e25
    [Google Scholar]
  63. Iggo A, Muir AR. 1969. The structure and function of a slowly adapting touch corpuscle in hairy skin. J. Physiol. 200:763–96
    [Google Scholar]
  64. Ito M, Liu Y, Yang Z, Nguyen J, Liang F et al. 2005. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat. Med. 11:1351–54
    [Google Scholar]
  65. Jacobson A, Yang D, Vella M, Chiu IM. 2021. The intestinal neuro-immune axis: crosstalk between neurons, immune cells, and microbes. Mucosal Immunol 14:555–65
    [Google Scholar]
  66. Jenkins BA, Fontecilla NM, Lu CP, Fuchs E, Lumpkin EA. 2019. The cellular basis of mechanosensory Merkel-cell innervation during development. eLife 8:e42633
    [Google Scholar]
  67. Joost S, Annusver K, Jacob T, Sun X, Dalessandri T et al. 2020. The molecular anatomy of mouse skin during hair growth and rest. Cell Stem Cell 26:441–57.e7
    [Google Scholar]
  68. Kamiya A, Hayama Y, Kato S, Shimomura A, Shimomura T et al. 2019. Genetic manipulation of autonomic nerve fiber innervation and activity and its effect on breast cancer progression. Nat. Neurosci. 22:1289–305
    [Google Scholar]
  69. Kanat O, Ertas H, Caner B. 2017. Platinum-induced neurotoxicity: a review of possible mechanisms. World J. Clin. Oncol. 8:329–35
    [Google Scholar]
  70. Karemaker JM. 2017. An introduction into autonomic nervous function. Physiol. Meas. 38:R89–118
    [Google Scholar]
  71. Kashem SW, Riedl MS, Yao C, Honda CN, Vulchanova L, Kaplan DH. 2015. Nociceptive sensory fibers drive interleukin-23 production from CD301b+ dermal dendritic cells and drive protective cutaneous immunity. Immunity 43:515–26
    [Google Scholar]
  72. Katayama Y, Battista M, Kao WM, Hidalgo A, Peired AJ et al. 2006. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124:407–21
    [Google Scholar]
  73. Keyes BE, Liu S, Asare A, Naik S, Levorse J et al. 2016. Impaired epidermal to dendritic T cell signaling slows wound repair in aged skin. Cell 167:1323–38.e14
    [Google Scholar]
  74. Keyes BE, Segal JP, Heller E, Lien W-H, Chang C-Y et al. 2013. Nfatc1 orchestrates aging in hair follicle stem cells. PNAS 110:E4950–59
    [Google Scholar]
  75. Knox SM, Lombaert IM, Haddox CL, Abrams SR, Cotrim A et al. 2013. Parasympathetic stimulation improves epithelial organ regeneration. Nat. Commun. 4:1494
    [Google Scholar]
  76. Knox SM, Lombaert IM, Reed X, Vitale-Cross L, Gutkind JS, Hoffman MP. 2010. Parasympathetic innervation maintains epithelial progenitor cells during salivary organogenesis. Science 329:1645–47
    [Google Scholar]
  77. Koizumi S, Fujishita K, Inoue K, Shigemoto-Mogami Y, Tsuda M, Inoue K. 2004. Ca2+ waves in keratinocytes are transmitted to sensory neurons: the involvement of extracellular ATP and P2Y2 receptor activation. Biochem. J. 380:329–38
    [Google Scholar]
  78. Lerner AB. 1966. Gray hair and sympathectomy. Report of a case. Arch. Dermatol. 93:235–36
    [Google Scholar]
  79. Li C-L, Li K-C, Wu D, Chen Y, Luo H et al. 2016. Somatosensory neuron types identified by high-coverage single-cell RNA-sequencing and functional heterogeneity. Cell Res. 26:83–102
    [Google Scholar]
  80. Li L, Rutlin M, Abraira VE, Cassidy C, Kus L et al. 2011. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147:1615–27
    [Google Scholar]
  81. Lin EE, Scott-Solomon E, Kuruvilla R. 2021. Peripheral innervation in the regulation of glucose homeostasis. Trends Neurosci. 44:189–202
    [Google Scholar]
  82. Liu Q, Vrontou S, Rice FL, Zylka MJ, Dong X, Anderson DJ 2007. Molecular genetic visualization of a rare subset of unmyelinated sensory neurons that may detect gentle touch. Nat. Neurosci. 10:946–48
    [Google Scholar]
  83. Liu S, Wang Z, Su Y, Qi L, Yang W et al. 2021. A neuroanatomical basis for electroacupuncture to drive the vagal-adrenal axis. Nature 598:641–45
    [Google Scholar]
  84. Liu S, Wang Z-F, Su Y-S, Ray RS, Jing X-H et al. 2020. Somatotopic organization and intensity dependence in driving distinct NPY-expressing sympathetic pathways by electroacupuncture. Neuron 108:436–50.e7
    [Google Scholar]
  85. Lu W-J, Mann RK, Nguyen A, Bi T, Silverstein M et al. 2018. Neuronal delivery of Hedgehog directs spatial patterning of taste organ regeneration. PNAS 115:E200–9
    [Google Scholar]
  86. Lu Z, Xie Y, Huang H, Jiang K, Zhou B et al. 2020. Hair follicle stem cells regulate retinoid metabolism to maintain the self-renewal niche for melanocyte stem cells. eLife 9:e52712
    [Google Scholar]
  87. Lucas D, Battista M, Shi PA, Isola L, Frenette PS. 2008. Mobilized hematopoietic stem cell yield depends on species-specific circadian timing. Cell Stem Cell 3:364–66
    [Google Scholar]
  88. Lucas D, Scheiermann C, Chow A, Kunisaki Y, Bruns I et al. 2013. Chemotherapy-induced bone marrow nerve injury impairs hematopoietic regeneration. Nat. Med. 19:695–703
    [Google Scholar]
  89. Luiz AP, MacDonald DI, Santana-Varela S, Millet Q, Sikandar S et al. 2019. Cold sensing by NaV1.8-positive and NaV1.8-negative sensory neurons. PNAS 116:3811–16
    [Google Scholar]
  90. Lumpkin EA, Caterina MJ. 2007. Mechanisms of sensory transduction in the skin. Nature 445:858–65
    [Google Scholar]
  91. Ma Q. 2020. Somato-autonomic reflexes of acupuncture. Med. Acupunct. 32:362–66
    [Google Scholar]
  92. Ma S, Zhang B, LaFave LM, Earl AS, Chiang Z et al. 2020. Chromatin potential identified by shared single-cell profiling of RNA and chromatin. Cell 183:1103–16.e20
    [Google Scholar]
  93. Mach DB, Rogers SD, Sabino MC, Luger NM, Schwei MJ et al. 2002. Origins of skeletal pain: sensory and sympathetic innervation of the mouse femur. Neuroscience 113:155–66
    [Google Scholar]
  94. Madeo M, Colbert PL, Vermeer DW, Lucido CT, Cain JT et al. 2018. Cancer exosomes induce tumor innervation. Nat. Commun. 9:4284
    [Google Scholar]
  95. Magnon C, Hall SJ, Lin J, Xue X, Gerber L et al. 2013. Autonomic nerve development contributes to prostate cancer progression. Science 341:1236361
    [Google Scholar]
  96. Maruyama K, Takayama Y, Sugisawa E, Yamanoi Y, Yokawa T et al. 2018. The ATP transporter VNUT mediates induction of dectin-1-triggered Candida nociception. iScience 6:306–18
    [Google Scholar]
  97. Maryanovich M, Zahalka AH, Pierce H, Pinho S, Nakahara F et al. 2018. Adrenergic nerve degeneration in bone marrow drives aging of the hematopoietic stem cell niche. Nat. Med. 24:782–91
    [Google Scholar]
  98. Massberg S, Schaerli P, Knezevic-Maramica I, Köllnberger M, Tubo N et al. 2007. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131:994–1008
    [Google Scholar]
  99. Matheis F, Muller PA, Graves CL, Gabanyi I, Kerner ZJ et al. 2020. Adrenergic signaling in muscularis macrophages limits infection-induced neuronal loss. Cell 180:64–78.e16
    [Google Scholar]
  100. Matteoli G, Gomez-Pinilla PJ, Nemethova A, Di Giovangiulio M, Cailotto C et al. 2014. A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen. Gut 63:938–48
    [Google Scholar]
  101. Mattiuz R, Wohn C, Ghilas S, Ambrosini M, Alexandre YO et al. 2018. Novel Cre-expressing mouse strains permitting to selectively track and edit type 1 conventional dendritic cells facilitate disentangling their complexity in vivo. Front. Immunol. 9:2805
    [Google Scholar]
  102. McKim DB, Patterson JM, Wohleb ES, Jarrett BL, Reader BF et al. 2016. Sympathetic release of splenic monocytes promotes recurring anxiety following repeated social defeat. Biol. Psychiatry 79:803–13
    [Google Scholar]
  103. McNees P, Meneses KD. 2007. Pressure ulcers and other chronic wounds in patients with and patients without cancer: a retrospective, comparative analysis of healing patterns. Ostomy Wound Manag. 53:70–78
    [Google Scholar]
  104. Melton LJ 3rd, Beard CM, Kokmen E, Atkinson EJ, O'Fallon WM. 1994. Fracture risk in patients with Alzheimer's disease. J. Am. Geriatr. Soc. 42:614–19
    [Google Scholar]
  105. Méndez-Ferrer S, Battista M, Frenette PS. 2010. Cooperation of β2- and β3-adrenergic receptors in hematopoietic progenitor cell mobilization. Ann. N.Y. Acad. Sci. 1192:139–44
    [Google Scholar]
  106. Méndez-Ferrer S, Lucas D, Battista M, Frenette PS. 2008. Haematopoietic stem cell release is regulated by circadian oscillations. Nature 452:442–47
    [Google Scholar]
  107. Meregnani J, Clarençon D, Vivier M, Peinnequin A, Mouret C et al. 2011. Anti-inflammatory effect of vagus nerve stimulation in a rat model of inflammatory bowel disease. Auton. Neurosci. 160:82–89
    [Google Scholar]
  108. Moen SM, Celius EG, Sandvik L, Nordsletten L, Eriksen EF, Holmøy T. 2011. Low bone mass in newly diagnosed multiple sclerosis and clinically isolated syndrome. Neurology 77:151–57
    [Google Scholar]
  109. Morrison KM, Miesegaes GR, Lumpkin EA, Maricich SM. 2009. Mammalian Merkel cells are descended from the epidermal lineage. Dev. Biol. 336:76–83
    [Google Scholar]
  110. Nakai A, Hayano Y, Furuta F, Noda M, Suzuki K. 2014. Control of lymphocyte egress from lymph nodes through β2-adrenergic receptors. J. Exp. Med. 211:2583–98
    [Google Scholar]
  111. Nguyen MB, Cohen I, Kumar V, Xu Z, Bar C et al. 2018. FGF signalling controls the specification of hair placode-derived SOX9 positive progenitors to Merkel cells. Nat. Commun. 9:2333
    [Google Scholar]
  112. Olson OC, Kang Y-A, Passegué E. 2020. Normal hematopoiesis is a balancing act of self-renewal and regeneration. Cold Spring Harb. . Perspect. Med. 10:a035519
    [Google Scholar]
  113. Ordovas-Montanes J, Rakoff-Nahoum S, Huang S, Riol-Blanco L, Barreiro O, von Andrian UH. 2015. The regulation of immunological processes by peripheral neurons in homeostasis and disease. Trends Immunol. 36:578–604
    [Google Scholar]
  114. Ortonne JP, Thivolet J, Guillet R. 1982. Graying of hair with age and sympathectomy. Arch. Dermatol. 118:876–77
    [Google Scholar]
  115. Pan Y, Hysinger JD, Barron T, Schindler NF, Cobb O et al. 2021. NF1 mutation drives neuronal activity-dependent initiation of optic glioma. Nature 594:277–82
    [Google Scholar]
  116. Patel A, Yamashita N, Ascaño M, Bodmer D, Boehm E et al. 2015. RCAN1 links impaired neurotrophin trafficking to aberrant development of the sympathetic nervous system in Down syndrome. Nat. Commun. 6:10119
    [Google Scholar]
  117. Perdigoto CN, Dauber KL, Bar C, Tsai P-C, Valdes VJ et al. 2016. Polycomb-mediated repression and Sonic hedgehog signaling interact to regulate Merkel cell specification during skin development. PLOS Genet. 12:e1006151
    [Google Scholar]
  118. Peterson SC, Eberl M, Vagnozzi AN, Belkadi A, Veniaminova NA et al. 2015. Basal cell carcinoma preferentially arises from stem cells within hair follicle and mechanosensory niches. Cell Stem Cell 16:400–12
    [Google Scholar]
  119. Pinho-Ribeiro FA, Baddal B, Haarsma R, O'Seaghdha M, Yang NJ et al. 2018. Blocking neuronal signaling to immune cells treats streptococcal invasive infection. Cell 173:1083–97.e22
    [Google Scholar]
  120. Powell ND, Sloan EK, Bailey MT, Arevalo JM, Miller GE et al. 2013. Social stress up-regulates inflammatory gene expression in the leukocyte transcriptome via β-adrenergic induction of myelopoiesis. PNAS 110:16574–79
    [Google Scholar]
  121. Rabbani P, Takeo M, Chou W, Myung P, Bosenberg M et al. 2011. Coordinated activation of Wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration. Cell 145:941–55
    [Google Scholar]
  122. Rabben H-L, Zhao C-M, Hayakawa Y, Wang TC, Chen D 2016. Vagotomy and gastric tumorigenesis. Curr. Neuropharmacol. 14:967–72
    [Google Scholar]
  123. Rachmin I, Lee JH, Zhang B, Sefton J, Jung I et al. 2021. Stress-associated ectopic differentiation of melanocyte stem cells and ORS amelanotic melanocytes in an ex vivo human hair follicle model. Exp. Dermatol. 30:578–87
    [Google Scholar]
  124. Riol-Blanco L, Ordovas-Montanes J, Perro M, Naval E, Thiriot A et al. 2014. Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation. Nature 510:157–61
    [Google Scholar]
  125. Scheiermann C, Kunisaki Y, Lucas D, Chow A, Jang JE et al. 2012. Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity 37:290–301
    [Google Scholar]
  126. Scott-Solomon E, Boehm E, Kuruvilla R. 2021. The sympathetic nervous system in development and disease. Nat. Rev. Neurosci. 22:685–702
    [Google Scholar]
  127. Seifert P, Spitznas M. 2002. Axons in human choroidal melanoma suggest the participation of nerves in the control of these tumors. Am. J. Ophthalmol. 133:711–13
    [Google Scholar]
  128. Shukla PK, Meena AS, Dalal K, Canelas C, Samak G et al. 2021. Chronic stress and corticosterone exacerbate alcohol-induced tissue injury in the gut-liver-brain axis. Sci. Rep. 11:826
    [Google Scholar]
  129. Shwartz Y, Gonzalez-Celeiro M, Chen C-L, Pasolli HA, Sheu S-H et al. 2020. Cell types promoting goosebumps form a niche to regulate hair follicle stem cells. Cell 182:578–93.e19
    [Google Scholar]
  130. Sipe LM, Yang C, Ephrem J, Garren E, Hirsh J, Deppmann CD. 2017. Differential sympathetic outflow to adipose depots is required for visceral fat loss in response to calorie restriction. Nutr. Diabetes 7:e260
    [Google Scholar]
  131. Sivamani RK, Pullar CE, Manabat-Hidalgo CG, Rocke DM, Carlsen RC et al. 2009. Stress-mediated increases in systemic and local epinephrine impair skin wound healing: potential new indication for beta blockers. PLOS Med. 6:e1000012
    [Google Scholar]
  132. Somers VK, Dyken ME, Mark AL, Abboud FM. 1993. Sympathetic-nerve activity during sleep in normal subjects. N. Engl. J. Med. 328:303–7
    [Google Scholar]
  133. Song H, Fang F, Tomasson G, Arnberg FK, Mataix-Cols D et al. 2018. Association of stress-related disorders with subsequent autoimmune disease. JAMA 319:2388–400
    [Google Scholar]
  134. Stachniak TJ, Ghosh A, Sternson SM. 2014. Chemogenetic synaptic silencing of neural circuits localizes a hypothalamus→midbrain pathway for feeding behavior. Neuron 82:797–808
    [Google Scholar]
  135. Stickels RR, Murray E, Kumar P, Li J, Marshall JL et al. 2021. Highly sensitive spatial transcriptomics at near-cellular resolution with Slide-seqV2. Nat. Biotechnol. 39:313–19
    [Google Scholar]
  136. Stirling LC, Forlani G, Baker MD, Wood JN, Matthews EA et al. 2005. Nociceptor-specific gene deletion using heterozygous NaV1.8-Cre recombinase mice. Pain 113:27–36
    [Google Scholar]
  137. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J et al. 2003. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–29
    [Google Scholar]
  138. Tam J, Trembovler V, Di Marzo V, Petrosino S, Leo G et al. 2008. The cannabinoid CB1 receptor regulates bone formation by modulating adrenergic signaling. FASEB J. 22:285–94
    [Google Scholar]
  139. Tanay A, Regev A. 2017. Scaling single-cell genomics from phenomenology to mechanism. Nature 541:331–38
    [Google Scholar]
  140. Tikhonova AN, Dolgalev I, Hu H, Sivaraj KK, Hoxha E et al. 2019. The bone marrow microenvironment at single-cell resolution. Nature 569:222–28
    [Google Scholar]
  141. Trier AM, Mack MR, Kim BS. 2019. The neuroimmune axis in skin sensation, inflammation, and immunity. J. Immunol. 202:2829–35
    [Google Scholar]
  142. Udit S, Blake K, Chiu IM. 2022. Somatosensory and autonomic neuronal regulation of the immune response. Nat. Rev. Neurosci. 23:157–71 https://doi.org/10.1038/s41583-021-00555-4
    [Crossref] [Google Scholar]
  143. Usoskin D, Furlan A, Islam S, Abdo H, Lönnerberg P et al. 2015. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Neurosci. 18:145–53
    [Google Scholar]
  144. Van Keymeulen A, Mascre G, Youseff KK, Harel I, Michaux C et al. 2009. Epidermal progenitors give rise to Merkel cells during embryonic development and adult homeostasis. J. Cell Biol. 187:91–100
    [Google Scholar]
  145. Veiga-Fernandes H, Mucida D. 2016. Neuro-immune interactions at barrier surfaces. Cell 165:801–11
    [Google Scholar]
  146. Venkatesh HS, Tam LT, Woo PJ, Lennon J, Nagaraja S et al. 2017. Targeting neuronal activity-regulated neuroligin-3 dependency in high-grade glioma. Nature 549:533–37
    [Google Scholar]
  147. Volmer-Thole M, Lobmann R. 2016. Neuropathy and diabetic foot syndrome. Int. J. Mol. Sci. 17:917
    [Google Scholar]
  148. Vrontou S, Wong AM, Rau KK, Koerber HR, Anderson DJ. 2013. Genetic identification of C fibres that detect massage-like stroking of hairy skin in vivo. Nature 493:669–73
    [Google Scholar]
  149. Wang LD, Wagers AJ. 2011. Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat. Rev. Mol. Cell Biol. 12:643–55
    [Google Scholar]
  150. Wu H, Williams J, Nathans J. 2012. Morphologic diversity of cutaneous sensory afferents revealed by genetically directed sparse labeling. eLife 1:e00181
    [Google Scholar]
  151. Xiao Y, Thoresen DT, Miao L, Williams JS, Wang C et al. 2016. A cascade of Wnt, Eda, and Shh signaling is essential for touch dome Merkel cell development. PLOS Genet. 12:e1006150
    [Google Scholar]
  152. Xiao Y, Thoresen DT, Williams JS, Wang C, Perna J et al. 2015. Neural Hedgehog signaling maintains stem cell renewal in the sensory touch dome epithelium. PNAS 112:7195–200
    [Google Scholar]
  153. Yirmiya R, Goshen I, Bajayo A, Kreisel T, Feldman S et al. 2006. Depression induces bone loss through stimulation of the sympathetic nervous system. PNAS 103:16876–81
    [Google Scholar]
  154. Zeng X, Ye M, Resch JM, Jedrychowski MP, Hu B et al. 2019. Innervation of thermogenic adipose tissue via a calsyntenin 3β–S100b axis. Nature 569:229–35
    [Google Scholar]
  155. Zhang B, Hsu Y-C. 2017. Emerging roles of transit – amplifying cells in tissue regeneration and cancer. Wiley Interdiscip. Rev. Dev. Biol. 6:wdev.282
    [Google Scholar]
  156. Zhang B, Ma S, Rachmin I, He M, Baral P et al. 2020. Hyperactivation of sympathetic nerves drives depletion of melanocyte stem cells. Nature 577:676–81
    [Google Scholar]
  157. Zhao Z-D, Yang WZ, Gao C, Fu X, Zhang W et al. 2017. A hypothalamic circuit that controls body temperature. PNAS 114:2042–47
    [Google Scholar]
  158. Zhou R, Deng J, Zhang M, Zhou H-D, Wang Y-J. 2011. Association between bone mineral density and the risk of Alzheimer's disease. J. Alzheimer's Dis. 24:101–8
    [Google Scholar]
  159. Zhou R, Zhou H, Rui L, Xu J. 2014. Bone loss and osteoporosis are associated with conversion from mild cognitive impairment to Alzheimer's disease. Curr. Alzheimer Res. 11:706–13
    [Google Scholar]
  160. Zylka MJ, Rice FL, Anderson DJ. 2005. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 45:17–25
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-120320-032429
Loading
/content/journals/10.1146/annurev-cellbio-120320-032429
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error