1932

Abstract

Dietary composition and calorie intake are major determinants of health and disease. Calorie restriction promotes metabolic changes that favor tissue regeneration and is arguably the most successful and best-conserved antiaging intervention. Obesity, in contrast, impairs tissue homeostasis and is a major risk factor for the development of diseases including cancer. Stem cells, the central mediators of tissue regeneration, integrate dietary and energy cues via nutrient-sensing pathways to maintain growth or respond to stress. We discuss emerging data on the effects of diet and nutrient-sensing pathways on intestinal stem cells, as well as their potential application in the development of regenerative and therapeutic interventions.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-nutr-082117-051644
2018-08-21
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/nutr/38/1/annurev-nutr-082117-051644.html?itemId=/content/journals/10.1146/annurev-nutr-082117-051644&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Amcheslavsky A, Ito N, Jiang J, Ip YT 2011. Tuberous sclerosis complex and Myc coordinate the growth and division of Drosophila intestinal stem cells. J. Cell Biol. 193:695–710
    [Google Scholar]
  2. 2.  Amcheslavsky A, Song W, Li Q, Nie Y, Bragatto I et al. 2014. Enteroendocrine cells support intestinal stem-cell-mediated homeostasis in Drosophila. Cell Rep 9:32–39
    [Google Scholar]
  3. 3.  Arendt LM, McCready J, Keller PJ, Baker DD, Naber SP et al. 2013. Obesity promotes breast cancer by CCL2-mediated macrophage recruitment and angiogenesis. Cancer Res 73:6080–93
    [Google Scholar]
  4. 4.  Baltgalvis KA, Berger FG, Peña MM, Davis JM, Carson JA 2009. The interaction of a high-fat diet and regular moderate intensity exercise on intestinal polyp development in Apc Min/+ mice. Cancer Prev. Res. 2:641–49
    [Google Scholar]
  5. 5.  Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H et al. 2009. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457:608–11
    [Google Scholar]
  6. 6.  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]
  7. 7.  Baron JA, Barry EL, Mott LA, Rees JR, Sandler RS et al. 2015. A trial of calcium and vitamin D for the prevention of colorectal adenomas. N. Engl. J. Med. 373:1519–30
    [Google Scholar]
  8. 8.  Beyaz S, Mana MD, Roper J, Kedrin D, Saadatpour A et al. 2016. High-fat diet enhances stemness and tumorigenicity of intestinal progenitors. Nature 531:53–58
    [Google Scholar]
  9. 9.  Bianchi G, Martella R, Ravera S, Marini C, Capitanio S et al. 2015. Fasting induces anti-Warburg effect that increases respiration but reduces ATP-synthesis to promote apoptosis in colon cancer models. Oncotarget 6:11806–19
    [Google Scholar]
  10. 10.  Bigarella CL, Liang R, Ghaffari S 2014. Stem cells and the impact of ROS signaling. Development 141:4206–18
    [Google Scholar]
  11. 11.  Blakeborough MH, Owen RW, Bilton RF 1989. Free radical generating mechanisms in the colon: their role in the induction and promotion of colorectal cancer?. Free Radic. Res. Commun. 6:359–67
    [Google Scholar]
  12. 12.  Blüher M, Kahn BB, Kahn CR 2003. Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299:572–74
    [Google Scholar]
  13. 13.  Bohane TD, Haka-Ikse K, Biggar WD, Hamilton JR, Gall DG 1979. A clinical study of young infants after small intestinal resection. J. Pediatr. 94:552–58
    [Google Scholar]
  14. 14.  Bonnet D, Dick JE 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3:730–37
    [Google Scholar]
  15. 15.  Boucher J, Kleinridders A, Kahn CR 2014. Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harb. Perspect. Biol 6:a009191
    [Google Scholar]
  16. 16.  Brandhorst S, Choi IY, Wei M, Cheng CW, Sedrakyan S et al. 2015. A periodic diet that mimics fasting promotes multi-system regeneration, enhanced cognitive performance, and healthspan. Cell Metab 22:86–99
    [Google Scholar]
  17. 17.  Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J et al. 2005. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. PNAS 102:3105–10
    [Google Scholar]
  18. 18.  Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P et al. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857–68
    [Google Scholar]
  19. 19.  Buchman AL, Moukarzel AA, Bhuta S, Belle M, Ament ME et al. 1995. Parenteral nutrition is associated with intestinal morphologic and functional changes in humans. J. Parenter. Enteral. Nutr. 19:453–60
    [Google Scholar]
  20. 20.  Buczacki SJ, Zecchini HI, Nicholson AM, Russell R, Vermeulen L et al. 2013. Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 495:65–69
    [Google Scholar]
  21. 21.  Cadwell K, Liu JY, Brown SL, Miyoshi H, Loh J et al. 2008. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456:259–63
    [Google Scholar]
  22. 22.  Calle EE, Kaaks R 2004. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4:579–91
    [Google Scholar]
  23. 23.  Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ 2003. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 348:1625–38
    [Google Scholar]
  24. 24.  Cerletti M, Jang YC, Finley LW, Haigis MC, Wagers AJ 2012. Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell 10:515–19
    [Google Scholar]
  25. 25.  Chen C, Liu Y, Liu R, Ikenoue T, Guan KL, Zheng P 2008. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J. Exp. Med. 205:2397–408
    [Google Scholar]
  26. 26.  Chen CL, Uthaya Kumar DB, Punj V, Xu J, Sher L et al. 2016. NANOG metabolically reprograms tumor-initiating stem-like cells through tumorigenic changes in oxidative phosphorylation and fatty acid metabolism. Cell Metab 23:206–19
    [Google Scholar]
  27. 27.  Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH 2008. Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 26:960–68
    [Google Scholar]
  28. 28.  Cheng CW, Adams GB, Perin L, Wei M, Zhou X et al. 2014. Prolonged fasting reduces IGF-1/PKA to promote hematopoietic-stem-cell-based regeneration and reverse immunosuppression. Cell Stem Cell 14:810–23
    [Google Scholar]
  29. 29.  Choi NH, Lucchetta E, Ohlstein B 2011. Nonautonomous regulation of Drosophila midgut stem cell proliferation by the insulin-signaling pathway. PNAS 108:18702–7
    [Google Scholar]
  30. 30.  Clevers H 2013. The intestinal crypt, a prototype stem cell compartment. Cell 154:274–84
    [Google Scholar]
  31. 31.  Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ et al. 2009. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325:201–4
    [Google Scholar]
  32. 32.  Dahly EM, Gillingham MB, Guo Z, Murali SG, Nelson DW et al. 2003. Role of luminal nutrients and endogenous GLP-2 in intestinal adaptation to mid-small bowel resection. Am. J. Physiol. Gastrointest. Liver Physiol. 284:G670–82
    [Google Scholar]
  33. 33.  Dallas NA, Xia L, Fan F, Gray MJ, Gaur P et al. 2009. Chemoresistant colorectal cancer cells, the cancer stem cell phenotype, and increased sensitivity to insulin-like growth factor-I receptor inhibition. Cancer Res 69:1951–57
    [Google Scholar]
  34. 34.  DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB 2008. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 7:11–20
    [Google Scholar]
  35. 35.  DeClercq V, McMurray DN, Chapkin RS 2015. Obesity promotes colonic stem cell expansion during cancer initiation. Cancer Lett 369:336–43
    [Google Scholar]
  36. 36.  Dekaney CM, Fong JJ, Rigby RJ, Lund PK, Henning SJ, Helmrath MA 2007. Expansion of intestinal stem cells associated with long-term adaptation following ileocecal resection in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 293:G1013–22
    [Google Scholar]
  37. 37.  Dekaney CM, Rodriguez JM, Graul MC, Henning SJ 2005. Isolation and characterization of a putative intestinal stem cell fraction from mouse jejunum. Gastroenterology 129:1567–80
    [Google Scholar]
  38. 38.  Deng H, Gerencser AA, Jasper H 2015. Signal integration by Ca2+ regulates intestinal stem-cell activity. Nature 528:212–17
    [Google Scholar]
  39. 39.  Esposito DL, Aru F, Lattanzio R, Morgano A, Abbondanza M et al. 2012. The insulin receptor substrate 1 (IRS1) in intestinal epithelial differentiation and in colorectal cancer. PLOS ONE 7:e36190
    [Google Scholar]
  40. 40.  Feldman EJ, Dowling RH, McNaughton J, Peters TJ 1976. Effects of oral versus intravenous nutrition on intestinal adaptation after small bowel resection in the dog. Gastroenterology 70:712–19
    [Google Scholar]
  41. 41.  Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S et al., eds. 2012. GLOBOCAN 2012: estimated cancer incidence, mortality and prevalence worldwide in 2012 IARC CancerBase No. 11, Lyon, France, v. 1.0. http://publications.iarc.fr/Databases/Iarc-Cancerbases/Globocan-2012-Estimated-Cancer-Incidence-Mortality-And-Prevalence-Worldwide-In-2012-V1-0-2012
  42. 42.  Firestein R, Blander G, Michan S, Oberdoerffer P, Ogino S et al. 2008. The SIRT1 deacetylase suppresses intestinal tumorigenesis and colon cancer growth. PLOS ONE 3:e2020
    [Google Scholar]
  43. 43.  Flachsbart F, Caliebe A, Kleindorp R, Blanché H, von Eller-Eberstein H et al. 2009. Association of FOXO3A variation with human longevity confirmed in German centenarians. PNAS 106:2700–5
    [Google Scholar]
  44. 44.  Fontana L, Partridge L, Longo VD 2010. Extending healthy life span—from yeast to humans. Science 328:321–26
    [Google Scholar]
  45. 45.  Ford ES 1999. Body mass index and colon cancer in a national sample of adult US men and women. Am. J. Epidemiol. 150:390–98
    [Google Scholar]
  46. 46.  Garland C, Shekelle RB, Barrett-Connor E, Criqui MH, Rossof AH, Paul O 1985. Dietary vitamin D and calcium and risk of colorectal cancer: a 19-year prospective study in men. Lancet 1:307–9
    [Google Scholar]
  47. 47.  Genovese G, Kähler AK, Handsaker RE, Lindberg J, Rose SA et al. 2014. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N. Engl. J. Med. 371:2477–87
    [Google Scholar]
  48. 48.  Haggar FA, Boushey RP 2009. Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clin. Colon Rectal Surg. 22:191–97
    [Google Scholar]
  49. 49.  Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM et al. 2009. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460:392–95
    [Google Scholar]
  50. 50.  Hernandez G, Velasco N, Wainstein C, Castillo L, Bugedo G et al. 1999. Gut mucosal atrophy after a short enteral fasting period in critically ill patients. J. Crit. Care 14:73–77
    [Google Scholar]
  51. 51.  Hochmuth CE, Biteau B, Bohmann D, Jasper H 2011. Redox regulation by Keap1 and Nrf2 controls intestinal stem cell proliferation in Drosophila. Cell Stem Cell 8:188–99
    [Google Scholar]
  52. 52.  Hoffmeister M, Bläker H, Kloor M, Roth W, Toth C et al. 2013. Body mass index and microsatellite instability in colorectal cancer: a population-based study. Cancer Epidemiol. Biomarkers Prev. 22:2303–11
    [Google Scholar]
  53. 53.  Holliday R 1989. Food, reproduction and longevity: Is the extended lifespan of calorie-restricted animals an evolutionary adaptation?. Bioessays 10:125–27
    [Google Scholar]
  54. 54.  Hritz I, Mandrekar P, Velayudham A, Catalano D, Dolganiuc A et al. 2008. The critical role of toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88. Hepatology 48:1224–31
    [Google Scholar]
  55. 55.  Hur JH, Bahadorani S, Graniel J, Koehler CL, Ulgherait M et al. 2013. Increased longevity mediated by yeast NDI1 expression in Drosophila intestinal stem and progenitor cells. Aging 5:662–81
    [Google Scholar]
  56. 56.  Igarashi M, Guarente L 2016. mTORC1 and SIRT1 cooperate to foster expansion of gut adult stem cells during calorie restriction. Cell 166:436–50
    [Google Scholar]
  57. 57.  Inoki K, Li Y, Zhu T, Wu J, Guan KL 2002. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4:648–57
    [Google Scholar]
  58. 58.  Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y et al. 2006. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126:955–68
    [Google Scholar]
  59. 59.  Inoki K, Zhu T, Guan KL 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577–90
    [Google Scholar]
  60. 60.  Ito K, Hirao A, Arai F, Takubo K, Matsuoka S et al. 2006. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat. Med. 12:446–51
    [Google Scholar]
  61. 61.  Jadhav U, Saxena M, O'Neill NK, Saadatpour A, Yuan GC et al. 2017. Dynamic reorganization of chromatin accessibility signatures during dedifferentiation of secretory precursors into Lgr5+ intestinal stem cells. Cell Stem Cell 21:65–77.e5
    [Google Scholar]
  62. 62.  Johnson IT, Lund EK 2007. Review article: nutrition, obesity and colorectal cancer. Aliment. Pharmacol. Ther. 26:161–81
    [Google Scholar]
  63. 63.  Kakuni M, Morimura K, Wanibuchi H, Ogawa M, Min W et al. 2002. Food restriction inhibits the growth of intestinal polyps in multiple intestinal neoplasia mouse. Jpn. J. Cancer Res. 93:236–41
    [Google Scholar]
  64. 64.  Kalaany NY, Sabatini DM 2009. Tumours with PI3K activation are resistant to dietary restriction. Nature 458:725–31
    [Google Scholar]
  65. 65.  Kapuria S, Karpac J, Biteau B, Hwangbo D, Jasper H 2012. Notch-mediated suppression of TSC2 expression regulates cell differentiation in the Drosophila intestinal stem cell lineage. PLOS Genet 8:e1003045
    [Google Scholar]
  66. 66.  Karunanithi S, Levi L, DeVecchio J, Karagkounis G, Reizes O et al. 2017. RBP4-STRA6 pathway drives cancer stem cell maintenance and mediates high-fat diet-induced colon carcinogenesis. Stem Cell Rep 9:438–50
    [Google Scholar]
  67. 67.  Katajisto P, Döhla J, Chaffer CL, Pentinmikko N, Marjanovic N et al. 2015. Stem cells. Asymmetric apportioning of aged mitochondria between daughter cells is required for stemness. Science 348:340–43
    [Google Scholar]
  68. 68.  Kim J, Kundu M, Viollet B, Guan KL 2011. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13:132–41
    [Google Scholar]
  69. 69.  Kim TH, Li F, Ferreiro-Neira I, Ho LL, Luyten A et al. 2014. Broadly permissive intestinal chromatin underlies lateral inhibition and cell plasticity. Nature 506:511–15
    [Google Scholar]
  70. 70.  Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T et al. 1994. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367:645–48
    [Google Scholar]
  71. 71.  Laplante M, Sabatini DM 2012. mTOR signaling in growth control and disease. Cell 149:274–93
    [Google Scholar]
  72. 72.  Lappe J, Watson P, Travers-Gustafson D, Recker R, Garland C et al. 2017. Effect of vitamin D and calcium supplementation on cancer incidence in older women: a randomized clinical trial. JAMA 317:1234–43
    [Google Scholar]
  73. 73.  Lee DF, Kuo HP, Chen CT, Hsu JM, Chou CK et al. 2007. IKKβ suppression of TSC1 links inflammation and tumor angiogenesis via the mTOR pathway. Cell 130:440–55
    [Google Scholar]
  74. 74.  Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villén J et al. 2006. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125:987–1001
    [Google Scholar]
  75. 75.  Liberti MV, Locasale JW 2016. The Warburg effect: How does it benefit cancer cells?. Trends Biochem. Sci. 41:211–18
    [Google Scholar]
  76. 76.  Lopez-Garcia C, Klein AM, Simons BD, Winton DJ 2010. Intestinal stem cell replacement follows a pattern of neutral drift. Science 330:822–25
    [Google Scholar]
  77. 77.  López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G 2013. The hallmarks of aging. Cell 153:1194–217
    [Google Scholar]
  78. 78.  Ma J, Pollak MN, Giovannucci E, Chan JM, Tao Y et al. 1999. Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (IGF)-I and IGF-binding protein-3. J. Natl. Cancer Inst. 91:620–25
    [Google Scholar]
  79. 79.  Mah AT, Van Landeghem L, Gavin HE, Magness ST, Lund PK 2014. Impact of diet-induced obesity on intestinal stem cells: hyperproliferation but impaired intrinsic function that requires insulin/IGF1. Endocrinology 155:3302–14
    [Google Scholar]
  80. 80.  Mai V, Colbert LH, Berrigan D, Perkins SN, Pfeiffer R et al. 2003. Calorie restriction and diet composition modulate spontaneous intestinal tumorigenesis in ApcMin mice through different mechanisms. Cancer Res 63:1752–55
    [Google Scholar]
  81. 81.  Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R et al. 2007. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6:458–71
    [Google Scholar]
  82. 82.  Masoro EJ 2003. Subfield history: caloric restriction, slowing aging, and extending life. Sci. Aging Knowledge Environ. 2003:RE2
    [Google Scholar]
  83. 83.  Massey DC, Bredin F, Parkes M 2008. Use of sirolimus (rapamycin) to treat refractory Crohn's disease. Gut 57:1294–96
    [Google Scholar]
  84. 84.  Mattison JA, Colman RJ, Beasley TM, Allison DB, Kemnitz JW et al. 2017. Caloric restriction improves health and survival of rhesus monkeys. Nat. Commun. 8:14063
    [Google Scholar]
  85. 85.  Mattison JA, Roth GS, Beasley TM, Tilmont EM, Handy AM et al. 2012. Impact of caloric restriction on health and survival in rhesus monkeys from the NIA study. Nature 489:318–21
    [Google Scholar]
  86. 86.  McCay CM, Crowell MF, Maynard LA 1989 (1935). The effect of retarded growth upon the length of life span and upon the ultimate body size. Nutrition 5:155–71
    [Google Scholar]
  87. 87.  McLeod CJ, Wang L, Wong C, Jones DL 2010. Stem cell dynamics in response to nutrient availability. Curr. Biol. 20:2100–5
    [Google Scholar]
  88. 88.  Meacham CE, Morrison SJ 2013. Tumour heterogeneity and cancer cell plasticity. Nature 501:328–37
    [Google Scholar]
  89. 89.  Mihaylova MM, Sabatini DM, Yilmaz Ö 2014. Dietary and metabolic control of stem cell function in physiology and cancer. Cell Stem Cell 14:292–305
    [Google Scholar]
  90. 90.  Miyamoto K, Araki KY, Naka K, Arai F, Takubo K et al. 2007. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 1:101–12
    [Google Scholar]
  91. 91.  Montgomery RK, Carlone DL, Richmond CA, Farilla L, Kranendonk ME et al. 2011. Mouse telomerase reverse transcriptase (mTert) expression marks slowly cycling intestinal stem cells. PNAS 108:179–84
    [Google Scholar]
  92. 92.  Moore SR, Guedes MM, Costa TB, Vallance J, Maier EA et al. 2015. Glutamine and alanyl-glutamine promote crypt expansion and mTOR signaling in murine enteroids. Am. J. Physiol. Gastrointest. Liver Physiol. 308:G831–39
    [Google Scholar]
  93. 93.  Morrison CD, Pistell PJ, Ingram DK, Johnson WD, Liu Y et al. 2010. High fat diet increases hippocampal oxidative stress and cognitive impairment in aged mice: implications for decreased Nrf2 signaling. J. Neurochem. 114:1581–89
    [Google Scholar]
  94. 94.  Mutalib M, Borrelli O, Blackstock S, Kiparissi F, Elawad M et al. 2014. The use of sirolimus (rapamycin) in the management of refractory inflammatory bowel disease in children. J. Crohns Colitis 8:1730–34
    [Google Scholar]
  95. 95.  Muñoz J, Stange DE, Schepers AG, van de Wetering M, Koo BK et al. 2012. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent ‘+4’ cell markers. EMBO J 31:3079–91
    [Google Scholar]
  96. 96.  Myant KB, Cammareri P, McGhee EJ, Ridgway RA, Huels DJ et al. 2013. ROS production and NF-κB activation triggered by RAC1 facilitate WNT-driven intestinal stem cell proliferation and colorectal cancer initiation. Cell Stem Cell 12:761–73
    [Google Scholar]
  97. 97. Natl. Cancer Inst. 2016. Cancer stat facts: colon and rectum cancer Rep., Natl. Cancer Inst Rockville, MD:
  98. 98.  Nieman KM, Kenny HA, Penicka CV, Ladanyi A, Buell-Gutbrod R et al. 2011. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nat. Med. 17:1498–503
    [Google Scholar]
  99. 99.  O'Brien LE, Soliman SS, Li X, Bilder D 2011. Altered modes of stem cell division drive adaptive intestinal growth. Cell 147:603–14
    [Google Scholar]
  100. 100.  Owusu-Ansah E, Banerjee U 2009. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 461:537–41
    [Google Scholar]
  101. 101.  Pascual G, Avgustinova A, Mejetta S, Martín M, Castellanos A et al. 2017. Targeting metastasis-initiating cells through the fatty acid receptor CD36. Nature 541:41–45
    [Google Scholar]
  102. 102.  Peregrina K, Houston M, Daroqui C, Dhima E, Sellers RS, Augenlicht LH 2015. Vitamin D is a determinant of mouse intestinal Lgr5 stem cell functions. Carcinogenesis 36:25–31
    [Google Scholar]
  103. 103.  Pietrocola F, Pol J, Vacchelli E, Rao S, Enot DP et al. 2016. Caloric restriction mimetics enhance anticancer immunosurveillance. Cancer Cell 30:147–60
    [Google Scholar]
  104. 104.  Porstmann T, Santos CR, Griffiths B, Cully M, Wu M et al. 2008. SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab 8:224–36
    [Google Scholar]
  105. 105.  Potten CS, Booth C, Tudor GL, Booth D, Brady G et al. 2003. Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation 71:28–41
    [Google Scholar]
  106. 106.  Powell AE, Wang Y, Li Y, Poulin EJ, Means AL et al. 2012. The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell 149:146–58
    [Google Scholar]
  107. 107.  Pugh TD, Oberley TD, Weindruch R 1999. Dietary intervention at middle age: caloric restriction but not dehydroepiandrosterone sulfate increases lifespan and lifetime cancer incidence in mice. Cancer Res 59:1642–48
    [Google Scholar]
  108. 108.  Pálmer HG, González-Sancho JM, Espada J, Berciano MT, Puig I et al. 2001. Vitamin D3 promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition of β-catenin signaling. J. Cell Biol. 154:369–87
    [Google Scholar]
  109. 109.  Rera M, Bahadorani S, Cho J, Koehler CL, Ulgherait M et al. 2011. Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog. Cell Metab 14:623–34
    [Google Scholar]
  110. 110.  Rera M, Clark RI, Walker DW 2012. Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. PNAS 109:21528–33
    [Google Scholar]
  111. 111.  Richmond CA, Shah MS, Deary LT, Trotier DC, Thomas H et al. 2015. Dormant intestinal stem cells are regulated by PTEN and nutritional status. Cell Rep 13:2403–11
    [Google Scholar]
  112. 112.  Rodríguez-Colman MJ, Schewe M, Meerlo M, Stigter E, Gerrits J et al. 2017. Interplay between metabolic identities in the intestinal crypt supports stem cell function. Nature 543:424–27
    [Google Scholar]
  113. 113.  Rossi DJ, Jamieson CH, Weissman IL 2008. Stems cells and the pathways to aging and cancer. Cell 132:681–96
    [Google Scholar]
  114. 114.  Sangiorgi E, Capecchi MR 2008. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 40:915–20
    [Google Scholar]
  115. 115.  Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG et al. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469:415–18
    [Google Scholar]
  116. 116.  Saxton RA, Sabatini DM 2017. mTOR signaling in growth, metabolism, and disease. Cell 169:361–71
    [Google Scholar]
  117. 117.  Scartozzi M, Mandolesi A, Giampieri R, Pierantoni C, Loupakis F et al. 2010. Insulin-like growth factor 1 expression correlates with clinical outcome in K-RAS wild type colorectal cancer patients treated with cetuximab and irinotecan. Int. J. Cancer 127:1941–47
    [Google Scholar]
  118. 118.  Schwitalla S, Fingerle AA, Cammareri P, Nebelsiek T, Göktuna SI et al. 2013. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152:25–38
    [Google Scholar]
  119. 119.  Sclafani F, Kim TY, Cunningham D, Kim TW, Tabernero J et al. 2015. A randomized phase II/III study of dalotuzumab in combination with cetuximab and irinotecan in chemorefractory, KRAS wild-type, metastatic colorectal cancer. J. Natl. Cancer Inst. 107:djv258
    [Google Scholar]
  120. 120.  Shestov AA, Liu X, Ser Z, Cluntun AA, Hung YP et al. 2014. Quantitative determinants of aerobic glycolysis identify flux through the enzyme GAPDH as a limiting step. eLife 3:e03342
    [Google Scholar]
  121. 121.  Snippert HJ, Schepers AG, van Es JH, Simons BD, Clevers H 2014. Biased competition between Lgr5 intestinal stem cells driven by oncogenic mutation induces clonal expansion. EMBO Rep 15:62–69
    [Google Scholar]
  122. 122.  Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M et al. 2010. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143:134–44
    [Google Scholar]
  123. 123.  Takeda N, Jain R, LeBoeuf MR, Wang Q, Lu MM, Epstein JA 2011. Interconversion between intestinal stem cell populations in distinct niches. Science 334:1420–24
    [Google Scholar]
  124. 124.  Taksler G 2017. Life-years lost to preventable causes-of-death in the US Paper presented at Annual Meeting of the Society of General Internal Medicine Washington, DC: Apr 19–22
  125. 125.  Takubo K, Nagamatsu G, Kobayashi CI, Nakamura-Ishizu A, Kobayashi H et al. 2013. Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell 12:49–61
    [Google Scholar]
  126. 126.  Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS 2001. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107–10
    [Google Scholar]
  127. 127.  Tetteh PW, Basak O, Farin HF, Wiebrands K, Kretzschmar K et al. 2016. Replacement of lost Lgr5-positive stem cells through plasticity of their enterocyte-lineage daughters. Cell Stem Cell 18:203–13
    [Google Scholar]
  128. 128.  Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Sabatini DM 2012. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485:109–13
    [Google Scholar]
  129. 129.  Tian H, Biehs B, Warming S, Leong KG, Rangell L et al. 2011. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478:255–59
    [Google Scholar]
  130. 130.  Tinkum KL, Stemler KM, White LS, Loza AJ, Jeter-Jones S et al. 2015. Fasting protects mice from lethal DNA damage by promoting small intestinal epithelial stem cell survival. PNAS 112:E7148–54
    [Google Scholar]
  131. 131.  Tomasetti C, Li L, Vogelstein B 2017. Stem cell divisions, somatic mutations, cancer etiology, and cancer prevention. Science 355:1330–34
    [Google Scholar]
  132. 132.  Tomasetti C, Vogelstein B 2015. Cancer etiology. Variation in cancer risk among tissues can be explained by the number of stem cell divisions. Science 347:78–81
    [Google Scholar]
  133. 133.  Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH et al. 2007. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128:325–39
    [Google Scholar]
  134. 134.  Tsao JL, Dudley S, Kwok B, Nickel AE, Laird PW et al. 2002. Diet, cancer and aging in DNA mismatch repair deficient mice. Carcinogenesis 23:1807–10
    [Google Scholar]
  135. 135.  Uthaya Kumar DB, Chen CL, Liu JC, Feldman DE, Sher LS et al. 2016. TLR4 signaling via NANOG cooperates with STAT3 to activate Twist1 and promote formation of tumor-initiating stem-like cells in livers of mice. Gastroenterology 150:707–19
    [Google Scholar]
  136. 136.  van der Flier LG, Haegebarth A, Stange DE, van de Wetering M, Clevers H 2009. OLFM4 is a robust marker for stem cells in human intestine and marks a subset of colorectal cancer cells. Gastroenterology 137:15–17
    [Google Scholar]
  137. 137.  van der Flier LG, van Gijn ME, Hatzis P, Kujala P, Haegebarth A et al. 2009. Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136:903–12
    [Google Scholar]
  138. 138.  van der Hulst RR, van Kreel BK, von Meyenfeldt MF, Brummer RJ, Arends JW et al. 1993. Glutamine and the preservation of gut integrity. Lancet 341:1363–65
    [Google Scholar]
  139. 139.  van Es JH, Sato T, van de Wetering M, Lyubimova A, Gregorieff A et al. 2012. Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol. 14:1099–104
    [Google Scholar]
  140. 140.  Vander Heiden MG, Cantley LC, Thompson CB 2009. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324:1029–33
    [Google Scholar]
  141. 141.  Vermeulen L, Morrissey E, van der Heijden M, Nicholson AM, Sottoriva A et al. 2013. Defining stem cell dynamics in models of intestinal tumor initiation. Science 342:995–98
    [Google Scholar]
  142. 142.  Vermeulen L, Snippert HJ 2014. Stem cell dynamics in homeostasis and cancer of the intestine. Nat. Rev. Cancer 14:468–80
    [Google Scholar]
  143. 143.  Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC et al. 1988. Genetic alterations during colorectal-tumor development. N. Engl. J. Med. 319:525–32
    [Google Scholar]
  144. 144.  Wactawski-Wende J, Kotchen JM, Anderson GL, Assaf AR, Brunner RL et al. 2006. Calcium plus vitamin D supplementation and the risk of colorectal cancer. N. Engl. J. Med. 354:684–96
    [Google Scholar]
  145. 145.  Warburg O 1956. On the origin of cancer cells. Science 123:309–14
    [Google Scholar]
  146. 146.  Warr MR, Binnewies M, Flach J, Reynaud D, Garg T et al. 2013. FOXO3A directs a protective autophagy program in haematopoietic stem cells. Nature 494:323–27
    [Google Scholar]
  147. 147.  Webb AE, Brunet A 2014. FOXO transcription factors: key regulators of cellular quality control. Trends Biochem. Sci. 39:159–69
    [Google Scholar]
  148. 148.  Willett W 1989. The search for the causes of breast and colon cancer. Nature 338:389–94
    [Google Scholar]
  149. 149.  Wu L, Zhou B, Oshiro-Rapley N, Li M, Paulo JA et al. 2016. An ancient, unified mechanism for metformin growth inhibition in C. elegans and cancer. Cell 167:1705–18.e13
    [Google Scholar]
  150. 150.  Wu S, Powers S, Zhu W, Hannun YA 2016. Substantial contribution of extrinsic risk factors to cancer development. Nature 529:43–47
    [Google Scholar]
  151. 151.  Yan KS, Gevaert O, Zheng GXY, Anchang B, Probert CS et al. 2017. Intestinal enteroendocrine lineage cells possess homeostatic and injury-inducible stem cell activity. Cell Stem Cell 21:78–90.e6
    [Google Scholar]
  152. 152.  Yang K, Edelmann W, Fan K, Lau K, Leung D et al. 1998. Dietary modulation of carcinoma development in a mouse model for human familial adenomatous polyposis. Cancer Res 58:5713–17
    [Google Scholar]
  153. 153.  Yang K, Kurihara N, Fan K, Newmark H, Rigas B et al. 2008. Dietary induction of colonic tumors in a mouse model of sporadic colon cancer. Cancer Res 68:7803–10
    [Google Scholar]
  154. 154.  Yilmaz Ö, Katajisto P, Lamming DW, Gültekin Y, Bauer-Rowe KE et al. 2012. mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 486:490–95
    [Google Scholar]
  155. 155.  Zhang J, Khvorostov I, Hong JS, Oktay Y, Vergnes L et al. 2011. UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J 30:4860–73
    [Google Scholar]
  156. 156.  Zhao J, Zhai B, Gygi SP, Goldberg AL 2015. mTOR inhibition activates overall protein degradation by the ubiquitin proteasome system as well as by autophagy. PNAS 112:15790–97
    [Google Scholar]
/content/journals/10.1146/annurev-nutr-082117-051644
Loading
/content/journals/10.1146/annurev-nutr-082117-051644
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