1932

Abstract

Natural polyamines (spermidine and spermine) are small, positively charged molecules that are ubiquitously found within organisms and cells. They exert numerous (intra)cellular functions and have been implicated to protect against several age-related diseases. Although polyamine levels decline in a complex age-dependent, tissue-, and cell type–specific manner, they are maintained in healthy nonagenarians and centenarians. Increased polyamine levels, including through enhanced dietary intake, have been consistently linked to improved health and reduced overall mortality. In preclinical models, dietary supplementation with spermidine prolongs life span and health span. In this review, we highlight salient aspects of nutritional polyamine intake and summarize the current knowledge of organismal and cellular uptake and distribution of dietary (and gastrointestinal) polyamines and their impact on human health. We further summarize clinical and epidemiological studies of dietary polyamines.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-nutr-120419-015419
2020-08-21
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/nutr/40/1/annurev-nutr-120419-015419.html?itemId=/content/journals/10.1146/annurev-nutr-120419-015419&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abdellatif M, Sedej S, Carmona-Gutierrez D, Madeo F, Kroemer G 2018. Autophagy in cardiovascular aging. Circ. Res. 123:7803–24
    [Google Scholar]
  2. 2. 
    Abdulhussein AA, Wallace HM. 2014. Polyamines and membrane transporters. Amino Acids 46:3655–60
    [Google Scholar]
  3. 3. 
    Adao R. 2005. Bioactive amines and carbohydrate changes during ripening of ‘Prata’ banana (Musa acuminata × M. balbisiana). Food Chem 90:4705–11
    [Google Scholar]
  4. 4. 
    Aouida M, Leduc A, Poulin R, Ramotar D 2005. AGP2 encodes the major permease for high affinity polyamine import in Saccharomyces cerevisiae. . J. Biol. Chem 280:2524267–76
    [Google Scholar]
  5. 5. 
    Aouida M, Rubio-Texeira M, Thevelein JM, Poulin R, Ramotar D 2013. Agp2, a member of the yeast amino acid permease family, positively regulates polyamine transport at the transcriptional level. PLOS ONE 8:6e65717 Erratum. 2013. PLOS ONE 8(7). https://doi.org/10.1371/annotation/ff0ad3b6-fff4-4783-8c2e-968a95283ab8
    [Crossref] [Google Scholar]
  6. 6. 
    Atiya Ali M, Poortvliet E, Strömberg R, Yngve A 2011. Polyamines: total daily intake in adolescents compared to the intake estimated from the Swedish Nutrition Recommendations Objectified (SNO). Food Nutr. Res. 2011:55 https://doi.org/10.3402/fnr.v55i0.5455
    [Crossref] [Google Scholar]
  7. 7. 
    Atiya Ali M, Poortvliet E, Strömberg R, Yngve A 2011. Polyamines in foods: development of a food database. Food Nutr. Res. 2011:55 https://doi.org/10.3402/fnr.v55i0.5572
    [Crossref] [Google Scholar]
  8. 8. 
    Balasundaram D, Tabor CW, Tabor H 1991. Spermidine or spermine is essential for the aerobic growth of Saccharomyces cerevisiae. . PNAS 88:135872–76
    [Google Scholar]
  9. 9. 
    Bardócz S. 1995. Polyamines in food and their consequences for food quality and human health. Trends Food Sci. Technol. 6:10341–46
    [Google Scholar]
  10. 10. 
    Bardócz S, Duguid TJ, Brown DS, Grant G, Pusztai A et al. 1995. The importance of dietary polyamines in cell regeneration and growth. Br. J. Nutr. 73:6819–28
    [Google Scholar]
  11. 11. 
    Bardócz S, Grant G, Brown D, Ralph A, Pusztai A 1993. Polyamines in food—implications for growth and health. J. Nutr. Biochem. 4:266–71
    [Google Scholar]
  12. 12. 
    Basu Roy UK, Rial NS, Kachel KL, Gerner EW 2008. Activated K-RAS increases polyamine uptake in human colon cancer cells through modulation of caveolar endocytosis. Mol. Carcinog. 47:7538–53
    [Google Scholar]
  13. 13. 
    Belting M, Mani K, Jönsson M, Cheng F, Sandgren S et al. 2003. Glypican-1 is a vehicle for polyamine uptake in mammalian cells: a pivotal role for nitrosothiol-derived nitric oxide. J. Biol. Chem. 278:4747181–89
    [Google Scholar]
  14. 14. 
    Binh PNT, Soda K, Kawakami M 2010. Mediterranean diet and polyamine intake: possible contribution of increased polyamine intake to inhibition of age-associated disease. Nutr. Diet. Suppl. 3:1–7
    [Google Scholar]
  15. 15. 
    Binh PNT, Soda K, Maruyama C, Kawakami M 2010. Relationship between food polyamines and gross domestic product in association with longevity in Asian countries. Health 02:121390
    [Google Scholar]
  16. 16. 
    Blachowski S, Motyl T, Grzelkowska K, Kasterka M, Orzechowski A, Interewicz B 1994. Involvement of polyamines in epidermal growth factor (EGF), transforming growth factor (TGF)-α and -β1 action on culture of L6 and fetal bovine myoblasts. Int. J. Biochem. 26:7891–97
    [Google Scholar]
  17. 17. 
    Borges CV, Belin MAF, Amorim EP, Minatel IO, Monteiro GC et al. 2019. Bioactive amines changes during the ripening and thermal processes of bananas and plantains. Food Chem 298:125020
    [Google Scholar]
  18. 18. 
    Büttner S, Broeskamp F, Sommer C, Markaki M, Habernig L et al. 2014. Spermidine protects against α-synuclein neurotoxicity. Cell Cycle 13:243903–8
    [Google Scholar]
  19. 19. 
    Buyukuslu N, Hizli H, Esin K, Garipagaoglu M 2014. A cross-sectional study: nutritional polyamines in frequently consumed foods of the Turkish population. Foods 3:4541–57
    [Google Scholar]
  20. 20. 
    Carrillo C, Canepa GE, Algranati ID, Pereira CA 2006. Molecular and functional characterization of a spermidine transporter (TcPAT12) from Trypanosoma cruzi. Biochem. Biophys. Res. . Commun 344:3936–40
    [Google Scholar]
  21. 21. 
    Casero RA Jr., Stewart TM, Pegg AE 2018. Polyamine metabolism and cancer: treatments, challenges and opportunities. Nat. Rev. Cancer 18:11681–95
    [Google Scholar]
  22. 22. 
    Casti A, Orlandini G, Reali N, Bacciottini F, Vanelli M, Bernasconi S 1982. Pattern of blood polyamines in healthy subjects from infancy to the adult age. J. Endocrinol. Investig. 5:4263–66
    [Google Scholar]
  23. 23. 
    Chai N, Zhang H, Li L, Yu X, Liu Y et al. 2019. Spermidine prevents heart injury in neonatal rats exposed to intrauterine hypoxia by inhibiting oxidative stress and mitochondrial fragmentation. Oxidative Med. Cell. Longev 2019:5406468. Corrigendum. 2019. Oxidative Med. Cell. Longev. 2019:8695089
    [Google Scholar]
  24. 24. 
    Cheng M-L, Wang C-H, Shiao M-S, Liu M-H, Huang Y-Y et al. 2015. Metabolic disturbances identified in plasma are associated with outcomes in patients with heart failure: diagnostic and prognostic value of metabolomics. J. Am. Coll. Cardiol. 65:151509–20
    [Google Scholar]
  25. 25. 
    Choi YH, Park HY. 2012. Anti-inflammatory effects of spermidine in lipopolysaccharide-stimulated BV2 microglial cells. J. Biomed. Sci. 19:131
    [Google Scholar]
  26. 26. 
    Chrisam M, Pirozzi M, Castagnaro S, Blaauw B, Polishchuck R et al. 2015. Reactivation of autophagy by spermidine ameliorates the myopathic defects of collagen VI-null mice. Autophagy 11:122142–52
    [Google Scholar]
  27. 27. 
    Cipolla BG, Havouis R, Moulinoux JP 2007. Polyamine contents in current foods: a basis for polyamine reduced diet and a study of its long term observance and tolerance in prostate carcinoma patients. Amino Acids 33:2203–12
    [Google Scholar]
  28. 28. 
    Cooper KD, Shukla JB, Rennert OM 1978. Polyamine compartmentalization in various human disease states. Clin. Chim. Acta 82:11–7
    [Google Scholar]
  29. 29. 
    del Carmen Rodriguez S, López B, Chaves AR 2001. Effect of different treatments on the evolution of polyamines during refrigerated storage of eggplants. J. Agric. Food Chem. 49:104700–5
    [Google Scholar]
  30. 30. 
    Diler AS, Ziylan YZ, Uzum G, Lefauconnier JM, Seylaz J, Pinard E 2002. Passage of spermidine across the blood-brain barrier in short recirculation periods following global cerebral ischemia: effects of mild hyperthermia. Neurosci. Res. 43:4335–42
    [Google Scholar]
  31. 31. 
    dos Anjos Barros NV, de Moura Rocha M, Glória MBA, da Mora Araújo MA, dos Reis Moreira-Araújo RS et al. 2017. Effect of cooking on the bioactive compounds and antioxidant activity in grains cowpea cultivars. Rev. Ciênc. Agronôm. 48:5SPE824–31
    [Google Scholar]
  32. 32. 
    Eisenberg T, Abdellatif M, Schroeder S, Primessnig U, Stekovic S et al. 2016. Cardioprotection and lifespan extension by the natural polyamine spermidine. Nat. Med. 22:121428–38
    [Google Scholar]
  33. 33. 
    Eisenberg T, Büttner S, Kroemer G, Madeo F 2007. The mitochondrial pathway in yeast apoptosis. Apoptosis 12:51011–23
    [Google Scholar]
  34. 34. 
    Eisenberg T, Knauer H, Schauer A, Büttner S, Ruckenstuhl C et al. 2009. Induction of autophagy by spermidine promotes longevity. Nat. Cell Biol. 11:111305–14
    [Google Scholar]
  35. 35. 
    Eliassen KA, Reistad R, Risøen U, Rønning HF 2002. Dietary polyamines. Food Chem 78:3273–80
    [Google Scholar]
  36. 36. 
    Elmore BO, Bollinger JA, Dooley DM 2002. Human kidney diamine oxidase: heterologous expression, purification, and characterization. J. Biol. Inorg. Chem. 7:6565–79
    [Google Scholar]
  37. 37. 
    Erwin BG, Persson L, Pegg AE 1984. Differential inhibition of histone and polyamine acetylases by multisubstrate analogues. Biochemistry 23:184250–55
    [Google Scholar]
  38. 38. 
    Esatbeyoglu T, Ehmer A, Chaize D, Rimbach G 2016. Quantitative determination of spermidine in 50 German cheese samples on a core-shell column by high-performance liquid chromatography with a photodiode array detector using a fully validated method. J. Agric. Food Chem. 64:102105–11
    [Google Scholar]
  39. 39. 
    Fan J, Yang X, Li J, Shu Z, Dai J et al. 2017. Spermidine coupled with exercise rescues skeletal muscle atrophy from D-gal-induced aging rats through enhanced autophagy and reduced apoptosis via AMPK-FOXO3a signal pathway. Oncotarget 8:1117475–90
    [Google Scholar]
  40. 40. 
    Fashe TM, Keinänen TA, Grigorenko NA, Khomutov AR, Jänne J et al. 2010. Cutaneous application of α-methylspermidine activates the growth of resting hair follicles in mice. Amino Acids 38:2583–90
    [Google Scholar]
  41. 41. 
    Fernández ÁF, Bárcena C, Martínez-García GG, Tamargo-Gómez I, Suárez MF et al. 2017. Autophagy counteracts weight gain, lipotoxicity and pancreatic β-cell death upon hypercaloric pro-diabetic regimens. Cell Death Dis 8:8e2970
    [Google Scholar]
  42. 42. 
    Frake RA, Ricketts T, Menzies FM, Rubinsztein DC 2015. Autophagy and neurodegeneration. J. Clin. Investig. 125:165–74
    [Google Scholar]
  43. 43. 
    Fujita M, Fujita Y, Iuchi S, Yamada K, Kobayashi Y et al. 2012. Natural variation in a polyamine transporter determines paraquat tolerance in Arabidopsis. . PNAS 109:166343–47
    [Google Scholar]
  44. 44. 
    Fujita M, Shinozaki K. 2014. Identification of polyamine transporters in plants: Paraquat transport provides crucial clues. Plant Cell Physiol 55:5855–61
    [Google Scholar]
  45. 45. 
    Gamble LD, Hogarty MD, Liu X, Ziegler DS, Marshall G et al. 2012. Polyamine pathway inhibition as a novel therapeutic approach to treating neuroblastoma. Front. Oncol. 2:162
    [Google Scholar]
  46. 46. 
    Gamble LD, Purgato S, Murray J, Xiao L, Yu DMT et al. 2019. Inhibition of polyamine synthesis and uptake reduces tumor progression and prolongs survival in mouse models of neuroblastoma. Sci. Transl. Med. 11:477eaau1099
    [Google Scholar]
  47. 47. 
    García-Prat L, Martínez-Vicente M, Perdiguero E, Ortet L, Rodríguez-Ubreva J et al. 2016. Autophagy maintains stemness by preventing senescence. Nature 529:758437–42
    [Google Scholar]
  48. 48. 
    Goytia M, Hawel L, Dhulipala VL, Joseph SJ, Read TD, Shafer WM 2015. Characterization of a spermine/spermidine transport system reveals a novel DNA sequence duplication in Neisseria gonorrhoeae. FEMS Microbiol. Lett 362:16fnv125
    [Google Scholar]
  49. 49. 
    Guerra GP, Rubin MA, Mello CF 2016. Modulation of learning and memory by natural polyamines. Pharmacol. Res. 112:99–118
    [Google Scholar]
  50. 50. 
    Guo X, Harada C, Namekata K, Kimura A, Mitamura Y et al. 2011. Spermidine alleviates severity of murine experimental autoimmune encephalomyelitis. Investig. Ophthalmol. Vis. Sci. 52:52696–703
    [Google Scholar]
  51. 51. 
    Gupta VK, Pech U, Bhukel A, Fulterer A, Ender A et al. 2016. Spermidine suppresses age-associated memory impairment by preventing adverse increase of presynaptic active zone size and release. PLOS Biol 14:9e1002563
    [Google Scholar]
  52. 52. 
    Gupta VK, Scheunemann L, Eisenberg T, Mertel S, Bhukel A et al. 2013. Restoring polyamines protects from age-induced memory impairment in an autophagy-dependent manner. Nat. Neurosci. 16:101453–60
    [Google Scholar]
  53. 53. 
    Hasne M-P, Ullman B. 2005. Identification and characterization of a polyamine permease from the protozoan parasite Leishmania major. J. Biol. Chem 280:1515188–94
    [Google Scholar]
  54. 54. 
    Hernández-Jover T, Izquierdo-Pulido M, Veciana-Nogués MT, Mariné-Font A, Vidal-Carou MC 1997. Biogenic amine and polyamine contents in meat and meat products. J. Agric. Food Chem. 45:62098–102
    [Google Scholar]
  55. 55. 
    Hesterberg RS, Cleveland JL, Epling-Burnette PK 2018. Role of polyamines in immune cell functions. Med. Sci. 6:122
    [Google Scholar]
  56. 56. 
    Hiasa M, Miyaji T, Haruna Y, Takeuchi T, Harada Y et al. 2014. Identification of a mammalian vesicular polyamine transporter. Sci. Rep. 4:6836
    [Google Scholar]
  57. 57. 
    Hiramatsu K, Sugimoto M, Kamei S, Hoshino M, Kinoshita K et al. 1995. Determination of amounts of polyamines excreted in urine: demonstration of N1,N8-diacetylspermidine and N1N12-diacetylspermine as components commonly occurring in normal human urine. J. Biochem. 117:1107–12
    [Google Scholar]
  58. 58. 
    Hyvönen MT, Merentie M, Uimari A, Keinänen TA, Jänne J, Alhonen L 2007. Mechanisms of polyamine catabolism-induced acute pancreatitis. Biochem. Soc. Trans. 35:2326–30
    [Google Scholar]
  59. 59. 
    Igarashi K, Kashiwagi K. 2010. Characteristics of cellular polyamine transport in prokaryotes and eukaryotes. Plant Physiol. Biochem. 48:7506–12
    [Google Scholar]
  60. 60. 
    Igarashi K, Ueda S, Yoshida K, Kashiwagi K 2006. Polyamines in renal failure. Amino Acids 31:4477–83
    [Google Scholar]
  61. 61. 
    Ilmarinen P, Moilanen E, Erjefält JS, Kankaanranta H 2014. The polyamine spermine inhibits mitochondrial permeability transition (mPT) and apoptosis in human eosinophils. Eur. Respir. J. 44:Suppl. 58P3842
    [Google Scholar]
  62. 62. 
    Ilmarinen P, Moilanen E, Erjefält JS, Kankaanranta H 2015. The polyamine spermine promotes survival and activation of human eosinophils. J. Allergy Clin. Immunol. 136:2482–84.e11
    [Google Scholar]
  63. 63. 
    Ivanova S, Botchkina GI, Al-Abed Y, Meistrell M, Batliwalla F et al. 1998. Cerebral ischemia enhances polyamine oxidation: identification of enzymatically formed 3-aminopropanal as an endogenous mediator of neuronal and glial cell death. J. Exp. Med. 188:2327–40
    [Google Scholar]
  64. 64. 
    Järvinen A, Keinänen TA, Grigorenko NA, Khomutov AR, Uimari A et al. 2006. Guide molecule-driven stereospecific degradation of α-methylpolyamines by polyamine oxidase. J. Biol. Chem. 281:84589–95
    [Google Scholar]
  65. 65. 
    Kalač P. 2009. Recent advances in the research on biological roles of dietary polyamines in man. J. Appl. Biomed. 7:65–74
    [Google Scholar]
  66. 66. 
    Kalač P, Krausová P. 2005. A review of dietary polyamines: formation, implications for growth and health and occurrence in foods. Food Chem 90:1–2219–30
    [Google Scholar]
  67. 67. 
    Kalač P, Křıžek M, Pelikánová T, Langová M, Veškrna O 2005. Contents of polyamines in selected foods. Food Chem 90:4561–64
    [Google Scholar]
  68. 68. 
    Kalač P, Švecová S, Pelikánová T 2002. Levels of biogenic amines in typical vegetable products. Food Chem 77:3349–51
    [Google Scholar]
  69. 69. 
    Kawakita M, Hiramatsu K, Moriya S, Samejima K, Takahashi K 2015. N1,N12-diacetylspermine in human urine: performance as a tumor marker, quantification, production, and excretion. Polyamines: A Universal Molecular Nexus for Growth, Survival, and Specialized Metabolism T Kusano, H Suzuki 305–13 Tokyo: Springer
    [Google Scholar]
  70. 70. 
    Kibe R, Kurihara S, Sakai Y, Suzuki H, Ooga T et al. 2014. Upregulation of colonic luminal polyamines produced by intestinal microbiota delays senescence in mice. Sci. Rep. 4:4548
    [Google Scholar]
  71. 71. 
    Kiechl S, Pechlaner R, Willeit P, Notdurfter M, Paulweber B et al. 2018. Higher spermidine intake is linked to lower mortality: a prospective population-based study. Am. J. Clin. Nutr. 108:2371–80
    [Google Scholar]
  72. 72. 
    Kiechl S, Willeit J. 2019. In a nutshell: findings from the Bruneck Study. Gerontology 65:19–19
    [Google Scholar]
  73. 73. 
    Kim J. 2017. Spermidine rescues proximal tubular cells from oxidative stress and necrosis after ischemic acute kidney injury. Arch. Pharmacal Res. 40:101197–208
    [Google Scholar]
  74. 74. 
    Kitada Y, Muramatsu K, Toju H, Kibe R, Benno Y et al. 2018. Bioactive polyamine production by a novel hybrid system comprising multiple indigenous gut bacterial strategies. Sci. Adv. 4:6eaat0062
    [Google Scholar]
  75. 75. 
    Kozová M, Kalač P, Pelikánová T 2009. Contents of biologically active polyamines in chicken meat, liver, heart and skin after slaughter and their changes during meat storage and cooking. Food Chem 116:2419–25
    [Google Scholar]
  76. 76. 
    LaRocca TJ, Gioscia-Ryan RA, Hearon CM Jr., Seals DR 2013. The autophagy enhancer spermidine reverses arterial aging. Mech. Ageing Dev. 134:7-8314–20
    [Google Scholar]
  77. 77. 
    Larqué E, Sabater-Molina M, Zamora S 2007. Biological significance of dietary polyamines. Nutrition 23:187–95
    [Google Scholar]
  78. 78. 
    Lavizzari T, Veciana-Nogués MT, Bover-Cid S, Mariné-Font A, Vidal-Carou MC 2006. Improved method for the determination of biogenic amines and polyamines in vegetable products by ion-pair high-performance liquid chromatography. J. Chromatogr. A 1129:167–72
    [Google Scholar]
  79. 79. 
    Löser C. 2000. Polyamines in human and animal milk. Br. J. Nutr. 84:Suppl. 1S55–58
    [Google Scholar]
  80. 80. 
    Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L et al. 2013. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 38:4729–41
    [Google Scholar]
  81. 81. 
    Madeo F, Bauer MA, Carmona-Gutierrez D, Kroemer G 2019. Spermidine: a physiological autophagy inducer acting as an anti-aging vitamin in humans. Autophagy 15:1165–68
    [Google Scholar]
  82. 82. 
    Madeo F, Carmona-Gutierrez D, Hofer SJ, Kroemer G 2019. Caloric restriction mimetics against age-associated disease: targets, mechanisms, and therapeutic potential. Cell Metab 29:3592–610
    [Google Scholar]
  83. 83. 
    Madeo F, Eisenberg T, Pietrocola F, Kroemer G 2018. Spermidine in health and disease. Science 359:6374eaan2788
    [Google Scholar]
  84. 84. 
    Marchant P, Manneh VA, Blankenship J 1986. N1-acetylspermidine is not a substrate for N-acetylspermidine deacetylase. Biochim. Biophys. Acta 881:2297–99
    [Google Scholar]
  85. 85. 
    Masuko T, Kusama‐Eguchi K, Sakata K, Kusama T, Chaki S et al. 2003. Polyamine transport, accumulation, and release in brain. J. Neurochem. 84:3610–17
    [Google Scholar]
  86. 86. 
    Matsumoto M, Benno Y. 2007. The relationship between microbiota and polyamine concentration in the human intestine: a pilot study. Microbiol. Immunol. 51:125–35
    [Google Scholar]
  87. 87. 
    Matsumoto M, Kitada Y, Naito Y 2019. Endothelial function is improved by inducing microbial polyamine production in the gut: a randomized placebo-controlled trial. Nutrients 11:5E1188
    [Google Scholar]
  88. 88. 
    Matsumoto M, Kurihara S, Kibe R, Ashida H, Benno Y 2011. Longevity in mice is promoted by probiotic-induced suppression of colonic senescence dependent on upregulation of gut bacterial polyamine production. PLOS ONE 6:8e23652
    [Google Scholar]
  89. 89. 
    McDonald RE, Kushad MM. 1986. Accumulation of putrescine during chilling injury of fruits. Plant Physiol 82:1324–26
    [Google Scholar]
  90. 90. 
    Miao H, Ou J, Peng Y, Zhang X, Chen Y et al. 2016. Macrophage ABHD5 promotes colorectal cancer growth by suppressing spermidine production by SRM. Nat. Commun. 7:11716
    [Google Scholar]
  91. 91. 
    Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y et al. 2011. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 334:60621573–77
    [Google Scholar]
  92. 92. 
    Miller-Fleming L, Olin-Sandoval V, Campbell K, Ralser M 2015. Remaining mysteries of molecular biology: the role of polyamines in the cell. J. Mol. Biol. 427:213389–406
    [Google Scholar]
  93. 93. 
    Milovic V. 2001. Polyamines in the gut lumen: bioavailability and biodistribution. Eur. J. Gastroenterol. Hepatol. 13:91021–25
    [Google Scholar]
  94. 94. 
    Minois N, Carmona-Gutierrez D, Madeo F 2011. Polyamines in aging and disease. Aging 3:8716–32
    [Google Scholar]
  95. 95. 
    Minois N, Rockenfeller P, Smith TK, Carmona-Gutierrez D 2014. Spermidine feeding decreases age-related locomotor activity loss and induces changes in lipid composition. PLOS ONE 9:7e102435
    [Google Scholar]
  96. 96. 
    Mizuguchi H, Imamura I, Takemura M, Fukui H 1994. Purification and characterization of diamine oxidase (histaminase) from rat small intestine. J. Biochem. 116:3631–35
    [Google Scholar]
  97. 97. 
    Moret S, Smela D, Populin T, Conte LS 2005. A survey on free biogenic amine content of fresh and preserved vegetables. Food Chem 89:3355–61
    [Google Scholar]
  98. 98. 
    Moulinoux J-P, Le Calve M, Quemener V, Quash G 1984. In vitro studies on the entry of polyamines into normal red blood cells. Biochimie 66:5385–93
    [Google Scholar]
  99. 99. 
    Mulangi V, Phuntumart V, Aouida M, Ramotar D, Morris P 2012. Functional analysis of OsPUT1, a rice polyamine uptake transporter. Planta 235:11–11
    [Google Scholar]
  100. 100. 
    Muñoz-Esparza NC, Latorre-Moratalla ML, Comas-Basté O, Toro-Funes N, Veciana-Nogués MT, Vidal-Carou MC 2019. Polyamines in food. Front. Nutr. 6:108
    [Google Scholar]
  101. 101. 
    Nishibori N, Fujihara S, Akatuki T 2007. Amounts of polyamines in foods in Japan and intake by Japanese. Food Chem 100:2491–97
    [Google Scholar]
  102. 102. 
    Nishimura K, Shiina R, Kashiwagi K, Igarashi K 2006. Decrease in polyamines with aging and their ingestion from food and drink. J. Biochem. 139:181–90
    [Google Scholar]
  103. 103. 
    Noack J, Kleessen B, Proll J, Dongowski G, Blaut M 1998. Dietary guar gum and pectin stimulate intestinal microbial polyamine synthesis in rats. J. Nutr. 128:81385–91
    [Google Scholar]
  104. 104. 
    Nordestgaard BG, Varbo A. 2014. Triglycerides and cardiovascular disease. Lancet 384:9943626–35
    [Google Scholar]
  105. 105. 
    Novella‐Rodríguez S, Veciana‐Nogués MT, Izquierdo‐Pulido M, Vidal‐Carou MC 2003. Distribution of biogenic amines and polyamines in cheese. J. Food Sci. 68:3750–56
    [Google Scholar]
  106. 106. 
    Novella-Rodríguez S, Veciana-Nogués MT, Vidal-Carou MC 2000. Biogenic amines and polyamines in milks and cheeses by ion-pair high performance liquid chromatography. J. Agric. Food Chem. 48:115117–23
    [Google Scholar]
  107. 107. 
    Nowotarski SL, Woster PM, Casero RA Jr 2013. Polyamines and cancer: implications for chemotherapy and chemoprevention. Expert Rev. Mol. Med. 15:e3
    [Google Scholar]
  108. 108. 
    Okamoto A, Sugi E, Koizumi Y, Yanagida F, Udaka S 1997. Polyamine content of ordinary foodstuffs and various fermented foods. Biosci. Biotechnol. Biochem. 61:91582–84
    [Google Scholar]
  109. 109. 
    Osborne DL, Seidel ER. 1990. Gastrointestinal luminal polyamines: cellular accumulation and enterohepatic circulation. Am. J. Physiol. 258:4, Part 1G576–84
    [Google Scholar]
  110. 110. 
    Park MH, Igarashi K. 2013. Polyamines and their metabolites as diagnostic markers of human diseases. Biomol. Ther. 21:11–9
    [Google Scholar]
  111. 111. 
    Paul S, Kang SC. 2013. Natural polyamine inhibits mouse skin inflammation and macrophage activation. Inflamm. Res. 62:7681–88
    [Google Scholar]
  112. 112. 
    Pegg AE. 2013. Toxicity of polyamines and their metabolic products. Chem. Res. Toxicol. 26:121782–800
    [Google Scholar]
  113. 113. 
    Pegg AE. 2016. Functions of polyamines in mammals. J. Biol. Chem. 291:2914904–12
    [Google Scholar]
  114. 114. 
    Pegg AE, Casero RA Jr 2011. Current status of the polyamine research field. Methods Mol. Biol. 720:3–35
    [Google Scholar]
  115. 115. 
    Pegg AE, McCann PP. 1982. Polyamine metabolism and function. Am. J. Physiol. 243:5C212–21
    [Google Scholar]
  116. 116. 
    Pekar T, Wendzel A, Flak W, Kremer A, Pauschenwein-Frantsich S et al. 2020. Spermidine in dementia. Wien Klin. Wochenschr. 132:142–46
    [Google Scholar]
  117. 117. 
    Phadwal K, Alegre-Abarrategui J, Watson AS, Pike L, Anbalagan S et al. 2012. A novel method for autophagy detection in primary cells: impaired levels of macroautophagy in immunosenescent T cells. Autophagy 8:4677–89
    [Google Scholar]
  118. 118. 
    Pietrocola F, Pol J, Vacchelli E, Rao S, Enot DP et al. 2016. Caloric restriction mimetics enhance anticancer immunosurveillance. Cancer Cell 30:1147–60
    [Google Scholar]
  119. 119. 
    Płonka J, Michalski A. 2017. The influence of processing technique on the catecholamine and indolamine contents of fruits. J. Food Compos. Anal. 57:102–8
    [Google Scholar]
  120. 120. 
    Poulin R, Casero RA, Soulet D 2012. Recent advances in the molecular biology of metazoan polyamine transport. Amino Acids 42:2711–23
    [Google Scholar]
  121. 121. 
    Pucciarelli S, Moreschini B, Micozzi D, De Fronzo GS, Carpi FM et al. 2012. Spermidine and spermine are enriched in whole blood of nona/centenarians. Rejuvenation Res 15:6590–95
    [Google Scholar]
  122. 122. 
    Puleston DJ, Zhang H, Powell TJ, Lipina E, Sims S et al. 2014. Autophagy is a critical regulator of memory CD8+ T cell formation. eLife 3:e03706
    [Google Scholar]
  123. 123. 
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:728559–65
    [Google Scholar]
  124. 124. 
    Rader DJ, Hovingh GK. 2014. HDL and cardiovascular disease. Lancet 384:9943618–25
    [Google Scholar]
  125. 125. 
    Ramos-Molina B, Queipo-Ortuño MI, Lambertos A, Tinahones FJ, Peñafiel R 2019. Dietary and gut microbiota polyamines in obesity- and age-related diseases. Front. Nutr. 6:24
    [Google Scholar]
  126. 126. 
    Ramot Y, Marzani B, Pinto D, Kloepper JE, Paus R 2015. N1-methylspermidine, a stable spermidine analog, prolongs anagen and regulates epithelial stem cell functions in human hair follicles. Arch. Dermatol. Res. 307:9841–47
    [Google Scholar]
  127. 127. 
    Ramot Y, Pietilä M, Giuliani G, Rinaldi F, Alhonen L, Paus R 2010. Polyamines and hair: a couple in search of perfection. Exp. Dermatol. 19:9784–90
    [Google Scholar]
  128. 128. 
    Ramot Y, Tiede S, Bíró T, Abu Bakar MH, Sugawara K et al. 2011. Spermidine promotes human hair growth and is a novel modulator of human epithelial stem cell functions. PLOS ONE 6:7e22564
    [Google Scholar]
  129. 129. 
    Rinaldi F, Marzani B, Pinto D, Ramot Y 2017. A spermidine-based nutritional supplement prolongs the anagen phase of hair follicles in humans: a randomized, placebo-controlled, double-blind study. Dermatol. Pract. Concept. 7:417–21
    [Google Scholar]
  130. 130. 
    Saaid M, Saad B, Hashim NH, Mohamed Ali AS, Saleh MI 2009. Determination of biogenic amines in selected Malaysian food. Food Chem 113:41356–62
    [Google Scholar]
  131. 131. 
    Sadasivan SK, Vasamsetti B, Singh J, Marikunte VV, Oommen AM et al. 2014. Exogenous administration of spermine improves glucose utilization and decreases bodyweight in mice. Eur. J. Pharmacol. 729:94–99
    [Google Scholar]
  132. 132. 
    Sánchez-Jiménez F, Ruiz-Pérez MV, Urdiales JL, Medina MA 2013. Pharmacological potential of biogenic amine-polyamine interactions beyond neurotransmission. Br. J. Pharmacol. 170:14–16
    [Google Scholar]
  133. 133. 
    Sansbury BE, DeMartino AM, Xie Z, Brooks AC, Brainard RE et al. 2014. Metabolomic analysis of pressure-overloaded and infarcted mouse hearts. Circ. Heart Fail. 7:4634–42
    [Google Scholar]
  134. 134. 
    Scalabrino G, Ferioli ME. 1984. Polyamines in mammalian ageing: an oncological problem, too? A review. Mech. Ageing Dev. 26:2–3149–64
    [Google Scholar]
  135. 135. 
    Schwarz C, Stekovic S, Wirth M, Benson G, Royer P et al. 2018. Safety and tolerability of spermidine supplementation in mice and older adults with subjective cognitive decline. Aging 10:119–33
    [Google Scholar]
  136. 136. 
    Seiler N, Atanassov CL. 1994. The natural polyamines and the immune system. Prog. Drug Res. 43:87–141
    [Google Scholar]
  137. 137. 
    Seiler N, Dezeure F. 1990. Polyamine transport in mammalian cells. Int. J. Biochem. 22:3211–18
    [Google Scholar]
  138. 138. 
    Seiler N, Raul F. 2005. Polyamines and apoptosis. J. Cell. Mol. Med. 9:3623–42
    [Google Scholar]
  139. 139. 
    Serrano M, Pretel MT, Martínez-Madrid MC, Romojaro F, Riquelme F 1998. CO2 treatment of zucchini squash reduces chilling-induced physiological changes. J. Agric. Food Chem. 46:72465–68
    [Google Scholar]
  140. 140. 
    Sharma S, Kumar P, Deshmukh R 2018. Neuroprotective potential of spermidine against rotenone induced Parkinson's disease in rats. Neurochem. Int. 116:104–11
    [Google Scholar]
  141. 141. 
    Shin WW, Fong WF, Pang SF, Wong PC 1985. Limited blood-brain barrier transport of polyamines. J. Neurochem. 44:41056–59
    [Google Scholar]
  142. 142. 
    Silla Santos MH. 1996. Biogenic amines: their importance in foods. Int. J. Food Microbiol. 29:2–3213–31
    [Google Scholar]
  143. 143. 
    Silva CMG, Glória MBA. 2002. Bioactive amines in chicken breast and thigh after slaughter and during storage at 4 ± 1°C and in chicken-based meat products. Food Chem 78:2241–48
    [Google Scholar]
  144. 144. 
    Soda K. 2011. The mechanisms by which polyamines accelerate tumor spread. J. Exp. Clin. Cancer Res. 30:195
    [Google Scholar]
  145. 145. 
    Soda K, Dobashi Y, Kano Y, Tsujinaka S, Konishi F 2009. Polyamine-rich food decreases age-associated pathology and mortality in aged mice. Exp. Gerontol. 44:11727–32
    [Google Scholar]
  146. 146. 
    Soda K, Kano Y, Chiba F 2012. Food polyamine and cardiovascular disease—an epidemiological study. Glob. J. Health Sci. 4:6170–78
    [Google Scholar]
  147. 147. 
    Soda K, Kano Y, Chiba F, Koizumi K, Miyaki Y 2013. Increased polyamine intake inhibits age-associated alteration in global DNA methylation and 1,2-dimethylhydrazine-induced tumorigenesis. PLOS ONE 8:5e64357
    [Google Scholar]
  148. 148. 
    Soda K, Kano Y, Sakuragi M, Takao K, Lefor A, Konishi F 2009. Long-term oral polyamine intake increases blood polyamine concentrations. J. Nutr. Sci. Vitaminol. 55:4361–66
    [Google Scholar]
  149. 149. 
    Spizzirri UG, Restuccia D, Curcio M, Parisi OI, Iemma F, Picci N 2013. Determination of biogenic amines in different cheese samples by LC with evaporative light scattering detector. J. Food Comp. Anal. 29:143–51
    [Google Scholar]
  150. 150. 
    Tabor CW, Tabor H. 1984. Polyamines. Annu. Rev. Biochem. 53:749–90
    [Google Scholar]
  151. 151. 
    Tain LS, Jain C, Nespital T, Froehlich J, Hinze Y et al. 2020. Longevity in response to lowered insulin signaling requires glycine N-methyltransferase-dependent spermidine production. Aging Cell 19:1e13043
    [Google Scholar]
  152. 152. 
    Takeuchi T, Harada Y, Moriyama S, Furuta K, Tanaka S et al. 2017. Vesicular polyamine transporter mediates vesicular storage and release of polyamine from mast cells. J. Biol. Chem. 292:93909–18
    [Google Scholar]
  153. 153. 
    Teixeira D, Santaolaria ML, Meneu V, Alonso E 2002. Dietary arginine slightly and variably affects tissue polyamine levels in male Swiss albino mice. J. Nutr. 132:123715–20
    [Google Scholar]
  154. 154. 
    Thaulow E, Erikssen J, Sandvik L, Stormorken H, Cohn PF 1991. Blood platelet count and function are related to total and cardiovascular death in apparently healthy men. Circulation 84:2613–17
    [Google Scholar]
  155. 155. 
    Thomas T, Thomas TJ. 2001. Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell. Mol. Life Sci. 58:2244–58
    [Google Scholar]
  156. 156. 
    Tofalo R, Cocchi S, Suzzi G 2019. Polyamines and gut microbiota. Front. Nutr. 6:16
    [Google Scholar]
  157. 157. 
    Uda K, Tsujikawa T, Fujiyama Y, Bamba T 2003. Rapid absorption of luminal polyamines in a rat small intestine ex vivo model. J. Gastroenterol. Hepatol. 18:5554–59
    [Google Scholar]
  158. 158. 
    Uemura T, Kashiwagi K, Igarashi K 2005. Uptake of putrescine and spermidine by Gap1p on the plasma membrane in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun 328:41028–33
    [Google Scholar]
  159. 159. 
    Uemura T, Kashiwagi K, Igarashi K 2007. Polyamine uptake by DUR3 and SAM3 in Saccharomyces cerevisiae. J. Biol. Chem 282:107733–41
    [Google Scholar]
  160. 160. 
    Uemura T, Stringer DE, Blohm-Mangone KA, Gerner EW 2010. Polyamine transport is mediated by both endocytic and solute carrier transport mechanisms in the gastrointestinal tract. Am. J. Physiol. Gastrointest. Liver Physiol. 299:2G517–22
    [Google Scholar]
  161. 161. 
    Uemura T, Tachihara K, Tomitori H, Kashiwagi K, Igarashi K 2005. Characteristics of the polyamine transporter TPO1 and regulation of its activity and cellular localization by phosphorylation. J. Biol. Chem. 280:109646–52
    [Google Scholar]
  162. 162. 
    Uemura T, Yerushalmi HF, Tsaprailis G, Stringer DE, Pastorian KE et al. 2008. Identification and characterization of a diamine exporter in colon epithelial cells. J. Biol. Chem. 283:3926428–35
    [Google Scholar]
  163. 163. 
    Valero D, Serrano M, Martínez-Madrid MC, Riquelme F 1997. Polyamines, ethylene, and physicochemical changes in low-temperature-stored peach (Prunus persica L. Cv. Maycrest). J. Agric. Food Chem. 45:93406–10
    [Google Scholar]
  164. 164. 
    Valsamaki K, Michaelidou A, Polychroniadou A 2000. Biogenic amine production in feta cheese. Food Chem 71:2259–66
    [Google Scholar]
  165. 165. 
    van Veen S, Martin S, Van den Haute C, Benoy V, Lyons J et al. 2020. ATP13A2 deficiency disrupts lysosomal polyamine export. Nature 578:7795419–24
    [Google Scholar]
  166. 166. 
    Vargas AJ, Ashbeck EL, Wertheim BC, Wallace RB, Neuhouser ML et al. 2015. Dietary polyamine intake and colorectal cancer risk in postmenopausal women. Am. J. Clin. Nutr. 102:2411–19
    [Google Scholar]
  167. 167. 
    Vargas AJ, Wertheim BC, Gerner EW, Thomson CA, Rock CL, Thompson PA 2012. Dietary polyamine intake and risk of colorectal adenomatous polyps. Am. J. Clin. Nutr. 96:1133–41
    [Google Scholar]
  168. 168. 
    Vivó M, de Vera N, Cortés R, Mengod G, Camón L, Martínez E 2001. Polyamines in the basal ganglia of human brain. Influence of aging and degenerative movement disorders. Neurosci. Lett. 304:1–2107–11
    [Google Scholar]
  169. 169. 
    Wang I-F, Guo B-S, Liu Y-C, Wu C-C, Yang C-H et al. 2012. Autophagy activators rescue and alleviate pathogenesis of a mouse model with proteinopathies of the TAR DNA-binding protein 43. PNAS 109:3715024–29
    [Google Scholar]
  170. 170. 
    Wang Y, Casero RA Jr 2006. Mammalian polyamine catabolism: a therapeutic target, a pathological problem, or both. J. Biochem. 139:117–25
    [Google Scholar]
  171. 171. 
    Willett WC, Sampson L, Stampfer MJ, Rosner B, Bain C et al. 1985. Reproducibility and validity of a semiquantitative food frequency questionnaire. Am. J. Epidemiol. 122:151–65
    [Google Scholar]
  172. 172. 
    Wirth M, Benson G, Schwarz C, Köbe T, Grittner U et al. 2018. The effect of spermidine on memory performance in older adults at risk for dementia: a randomized controlled trial. Cortex 109:181–88
    [Google Scholar]
  173. 173. 
    Wirth M, Schwarz C, Benson G, Horn N, Buchert R et al. 2019. Effects of spermidine supplementation on cognition and biomarkers in older adults with subjective cognitive decline (SmartAge)—study protocol for a randomized controlled trial. Alzheimers Res. Ther. 11:136
    [Google Scholar]
  174. 174. 
    Yan J, Yan J-Y, Wang Y-X, Ling Y-N, Song X-D et al. 2019. Spermidine-enhanced autophagic flux improves cardiac dysfunction following myocardial infarction by targeting the AMPK/mTOR signalling pathway. Br. J. Pharmacol. 176:173126–42
    [Google Scholar]
  175. 175. 
    Yanagihara N, Moriwaki M, Shiraki K, Miki T, Otani S 1996. The involvement of polyamines in the proliferation of cultured retinal pigment epithelial cells. Investig. Ophthalmol. Vis. Sci. 37:101975–83
    [Google Scholar]
  176. 176. 
    Yang Q, Zheng C, Cao J, Cao G, Shou P et al. 2016. Spermidine alleviates experimental autoimmune encephalomyelitis through inducing inhibitory macrophages. Cell Death Differ 23:111850–61
    [Google Scholar]
  177. 177. 
    Yankah VV, Ohshima T, Koizumi C 1993. Effects of processing and storage on some chemical characteristics and lipid composition of a Ghanaian fermented fish product. J. Sci. Food Agric. 63:2227–35
    [Google Scholar]
  178. 178. 
    Yue F, Li W, Zou J, Jiang X, Xu G et al. 2017. Spermidine prolongs lifespan and prevents liver fibrosis and hepatocellular carcinoma by activating MAP1S-mediated autophagy. Cancer Res 77:112938–51
    [Google Scholar]
  179. 179. 
    Zhang H, Wang J, Li L, Chai N, Chen Y et al. 2017. Spermine and spermidine reversed age-related cardiac deterioration in rats. Oncotarget 8:3964793–808
    [Google Scholar]
  180. 180. 
    Zhang Y, Yin J, Zhang L, Qi C-C, Ma Z-L et al. 2017. Spermidine preconditioning ameliorates laurate-induced brain injury by maintaining mitochondrial stability. Neurol. Res. 39:3248–58
    [Google Scholar]
  181. 181. 
    Ziegler W, Hahn M, Wallnofer PR 1994. Changes in biogenic amine contents during processing of several plant foods. Dtsch. Lebensm. Rundsch. 90:108–12
    [Google Scholar]
  182. 182. 
    Zoumas-Morse C, Rock CL, Quintana EL, Neuhouser ML, Gerner EW, Meyskens FL Jr 2007. Development of a polyamine database for assessing dietary intake. J. Am. Diet. Assoc. 107:61024–27
    [Google Scholar]
/content/journals/10.1146/annurev-nutr-120419-015419
Loading
/content/journals/10.1146/annurev-nutr-120419-015419
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