Gastroenterology
Volume 137, Issue 1 , Pages 136-144.e3 , July 2009

Colony Stimulating Factor-1 Dependence of Paneth Cell Development in the Mouse Small Intestine

  • Duy Huynh

      Affiliations

    • Peter MacCallum Cancer Centre, East Melbourne, Australia
    • Department of Genetics, Latrobe University, Bundoora, Australia
    • ,
  • Xu–Ming Dai

      Affiliations

    • Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, New York, New York
    • ,
  • Sayan Nandi

      Affiliations

    • Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, New York, New York
    • ,
  • Sally Lightowler

      Affiliations

    • Peter MacCallum Cancer Centre, East Melbourne, Australia
    • ,
  • Melanie Trivett

      Affiliations

    • Peter MacCallum Cancer Centre, East Melbourne, Australia
    • ,
  • Chee–Kai Chan

      Affiliations

    • Department of Genetics, Latrobe University, Bundoora, Australia
    • ,
  • Ivan Bertoncello

      Affiliations

    • The Australian Stem Cell Centre, Clayton, Australia
    • ,
  • Robert G. Ramsay

      Affiliations

    • Peter MacCallum Cancer Centre, East Melbourne, Australia
    • Department of Pathology, the University of Melbourne, Parkville, Australia
    • Corresponding Author InformationReprint requests Address requests for reprints to: Robert G. Ramsay, Peter MacCallum Cancer Centre, St. Andrews Place, East Melbourne 3002, Australia. fax: (61) 3-9656-1411
    • ,
  • E. Richard Stanley

      Affiliations

    • Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, New York, New York
    • Corresponding Author InformationE. Richard Stanley, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, New York 10461. fax: (718) 430-8567

Received 8 July 2008 ,Accepted 10 March 2009.

References 

  1. Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine (V. Unitarian Theory of the origin of the four epithelial cell types). Am J Anat. 1974;141:537–561
  2. Potten CS. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci. 1998;353:821–830
  3. Potten CS. Radiation, the ideal cytotoxic agent for studying the cell biology of tissues such as the small intestine. Radiat Res. 2004;161:123–136
  4. Sancho E, Batlle E, Clevers H. Live and let die in the intestinal epithelium. Curr Opin Cell Biol. 2003;15:763–770
  5. Sancho E, Batlle E, Clevers H. Signaling pathways in intestinal development and cancer. Annu Rev Cell Dev Biol. 2004;20:695–723
  6. Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine (I. Columnar cell). Am J Anat. 1974;141:461–479
  7. Cheng H. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine (II. Mucous cells). Am J Anat. 1974;141:481–501
  8. Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine (III. Entero-endocrine cells). Am J Anat. 1974;141:503–519
  9. Hocker M, Raychowdhury R, Plath T, et al. Sp1 and CREB mediate gastrin-dependent regulation of chromogranin A promoter activity in gastric carcinoma cells. J Biol Chem. 1998;273:34000–34007
  10. Marshman E, Booth C, Potten CS. The intestinal epithelial stem cell. Bioessays. 2002;24:91–98
  11. Cheng H. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine (IV. Paneth cells). Am J Anat. 1974;141:521–535
  12. Cheng H, Merzel J, Leblond CP. Renewal of Paneth cells in the small intestine of the mouse. Am J Anat. 1969;126:507–525
  13. Elmes ME. The Paneth cell population of the small intestine of the rat-effects of fasting and zinc deficiency on total count and on dithizone-reactive count. J Pathol. 1976;118:183–191
  14. Troughton WD, Trier JS. Paneth and goblet cell renewal in mouse duodenal crypts. J Cell Biol. 1969;41:251–268
  15. Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003–1007
  16. Keshav S. Paneth cells: leukocyte-like mediators of innate immunity in the intestine. J Leukoc Biol. 2006;80:500–508
  17. Porter EM, Bevins CL, Ghosh D, Ganz T. The multifaceted Paneth cell. Cell Mol Life Sci. 2002;59:156–170
  18. Wehkamp J, Stange EF. Paneth cells and the innate immune response. Curr Opin Gastroenterol. 2006;22:644–650
  19. Huttner KM, Selsted ME, Ouellette AJ. Structure and diversity of the murine cryptdin gene family. Genomics. 1994;19:448–453
  20. Wilson CL, Heppner KJ, Rudolph LA, Matrisian LM. The metalloproteinase matrilysin is preferentially expressed by epithelial cells in a tissue-restricted pattern in the mouse. Mol Biol Cell. 1995;6:851–869
  21. Kiyohara H, Egami H, Shibata Y, Murata K, Ohshima S, Ogawa M. Light microscopic immunohistochemical analysis of the distribution of group II phospholipase A2 in human digestive organs. J Histochem Cytochem. 1992;40:1659–1664
  22. Satoh Y, Ishikawa K, Tanaka H, Oomori Y, Ono K. Immunohistochemical observations of lysozyme in the Paneth cells of specific-pathogen-free and germ-free mice. Acta Histochem. 1988;83:185–188
  23. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol. 2000;1:113–118
  24. Marks SC, Lane PW. Osteopetrosis, a new recessive skeletal mutation on chromosome 12 of the mouse. J Hered. 1976;67:11–18
  25. Cecchini MG, Dominguez MG, Mocci S, et al. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development. 1994;120:1357–1372
  26. Pollard JW, Stanley ER. Pleiotropic roles for CSF-1 in development defined by the mouse mutation osteopetrotic. Adv Dev Biochem. 1996;4:153–193
  27. Wiktor-Jedrzejczak W, Bartocci A, Ferrante AW, et al. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc Natl Acad Sci U S A. 1990;87:4828–4832
  28. Yoshida H, Hayashi S, Kunisada T, et al. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature. 1990;345:442–444
  29. Dai XM, Ryan GR, Hapel AJ, et al. Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood. 2002;99:111–120
  30. Dai XM, Zong XH, Akhter MP, Stanley ER. Osteoclast deficiency results in disorganized matrix, reduced mineralization, and abnormal osteoblast behavior in developing bone. J Bone Miner Res. 2004;19:1441–1451
  31. Ginhoux F, Tacke F, Angeli V, et al. Langerhans cells arise from monocytes in vivo. Nat Immunol. 2006;7:265–273
  32. Ryan GR, Dai XM, Dominguez MG, et al. Rescue of the colony-stimulating factor 1 (CSF-1)-nullizygous mouse (Csf1(op)/Csf1(op)) phenotype with a CSF-1 transgene and identification of sites of local CSF-1 synthesis. Blood. 2001;98:74–84
  33. Sudo T, Nishikawa S, Ogawa M, et al. Functional hierarchy of c-kit and c-fms in intramarrow production of CFU-M. Oncogene. 1995;11:2469–2476
  34. Murayama T, Yokode M, Kataoka H, et al. Intraperitoneal administration of anti-c-fms monoclonal antibody prevents initial events of atherogenesis but does not reduce the size of advanced lesions in apolipoprotein E-deficient mice. Circulation. 1999;99:1740–1746
  35. McLean IW, Nakane PK. Periodate-lysine-paraformaldehyde fixative (A new fixation for immunoelectron microscopy). J Histochem Cytochem. 1974;22:1077–1083
  36. Karlsson J, Putsep K, Chu H, Kays RJ, Bevins CL, Andersson M. Regional variations in Paneth cell antimicrobial peptide expression along the mouse intestinal tract. BMC Immunol. 2008;9:37
  37. Buscher D, Dello Sbarba P, et al. v-raf confers CSF-1 independent growth to a macrophage cell line and leads to immediate early gene expression without MAP-kinase activation. Oncogene. 1993;8:3323–3332
  38. Hennighausen L, Wall RJ, Tillmann U, Li M, Furth PA. Conditional gene expression in secretory tissues and skin of transgenic mice using the MMTV-LTR and the tetracycline responsive system. J Cell Biochem. 1995;59:463–472
  39. Whitehead RH, Demmler K, Rockman SP, Watson NK. Clonogenic growth of epithelial cells from normal colonic mucosa from both mice and humans. Gastroenterology. 1999;117:858–865
  40. Nandi S, Akhter MP, Seifert MF, Dai XM, Stanley ER. Developmental and functional significance of the CSF-1 proteoglycan chondroitin sulfate chain. Blood. 2006;107:786–795
  41. Owens SR, Greenson JK. The pathology of malabsorption: current concepts. Histopathology. 2007;50:64–82
  42. Sorokin SP, Hoyt RF. PAS-lead hematoxylin as a stain for small-granule endocrine cell populations in the lungs, other pharyngeal derivatives and the gut. Anat Rec. 1978;192:245–259
  43. Chung LP, Keshav S, Gordon S. Cloning the human lysozyme cDNA: inverted Alu repeat in the mRNA and in situ hybridization for macrophages and Paneth cells. Proc Natl Acad Sci U S A. 1988;85:6227–6231
  44. Matsushime H, Roussel MF, Ashmun RA, Sherr CJ. Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell. 1991;65:701–713
  45. Mathan M, Hughes J, Whitehead R. The morphogenesis of the human Paneth cell (An immunocytochemical ultrastructural study). Histochemistry. 1987;87:91–96
  46. Dai XM, Zong XH, Sylvestre V, Stanley ER. Incomplete restoration of colony-stimulating factor 1 (CSF-1) function in CSF-1-deficient Csf1op/Csf1op mice by transgenic expression of cell surface CSF-1. Blood. 2004;103:1114–1123
  47. Guleria I, Pollard JW. The trophoblast is a component of the innate immune system during pregnancy. Nat Med. 2000;6:589–593
  48. Chitu V, Stanley ER. Colony-stimulating factor-1 in immunity and inflammation. Curr Opin Immunol. 2006;18:39–48
  49. Garabedian EM, Roberts LJ, McNevin MS, Gordon JI. Examining the role of Paneth cells in the small intestine by lineage ablation in transgenic mice. J Biol Chem. 1997;272:23729–23740
  50. Lin EY, Gouon-Evans V, Nguyen AV, Pollard JW. The macrophage growth factor CSF-1 in mammary gland development and tumor progression. J Mammary Gland Biol Neoplasia. 2002;7:147–162
  51. Pull SL, Doherty JM, Mills JC, Gordon JI, Stappenbeck TS. Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc Natl Acad Sci U S A. 2005;102:99–104
  52. Goswami S, Sahai E, Wyckoff JB, et al. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res. 2005;65:5278–5283
  53. Hermiston ML, Wong MH, Gordon JI. Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system. Genes Dev. 1996;10:985–996
  54. Bienz M, Clevers H. Linking colorectal cancer to Wnt signaling. Cell. 2000;103:311–320
  55. Korinek V, Barker N, Moerer P, et al. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet. 1998;19:379–383
  56. Andreu P, Peignon G, Slomianny C, et al. A genetic study of the role of the Wnt/beta-catenin signalling in Paneth cell differentiation. Dev Biol. 2008;324:288–296
  57. Andreu P, Colnot S, Godard C, et al. Crypt-restricted proliferation and commitment to the Paneth cell lineage following Apc loss in the mouse intestine. Development. 2005;132:1443–1451
  58. van Es JH, van Gijn ME, Riccio O, et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature. 2005;435:959–963
  59. Lin H, Lee E, Hestir K, et al. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science. 2008;320:807–811
  60. Sweet MJ, Hume DA. CSF-1 as a regulator of macrophage activation and immune responses. Arch Immunol Ther Exp (Warsz). 2003;51:169–177
  61. Roth P, Bartocci A, Stanley ER. Lipopolysaccharide induces synthesis of mouse colony-stimulating factor-1 in vivo. J Immunol. 1997;158:3874–3880
  62. Adegboyega PA, Mifflin RC, DiMari JF, Saada JI, Powell DW. Immunohistochemical study of myofibroblasts in normal colonic mucosa, hyperplastic polyps, and adenomatous colorectal polyps. Arch Pathol Lab Med. 2002;126:829–836
  63. Marsh MN, Trier JS. Morphology and cell proliferation of subepithelial fibroblasts in adult mouse jejunum (II. Radioautographic studies). Gastroenterology. 1974;67:636–645
  64. Grimm MC, Pavli P. NOD2 mutations and Crohn's disease: are Paneth cells and their antimicrobial peptides the link?. Gut. 2004;53:1558–1560
  65. Wehkamp J, Harder J, Weichenthal M, et al. NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal alpha-defensin expression. Gut. 2004;53:1658–1664
  66. Wehkamp J, Schmid M, Fellermann K, Stange EF. Defensin deficiency, intestinal microbes, and the clinical phenotypes of Crohn's disease. J Leukoc Biol. 2005;77:460–465
  67. Wehkamp J, Schmid M, Stange EF. Defensins and other antimicrobial peptides in inflammatory bowel disease. Curr Opin Gastroenterol. 2007;23:370–378
  68. Ii M, Yamamoto H, Adachi Y, Maruyama Y, Shinomura Y. Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Exp Biol Med (Maywood). 2006;231:20–27
  69. Marshall D, Cameron J, Lightwood D, Lawson AD. Blockade of colony stimulating factor-1 (CSF-I) leads to inhibition of DSS-induced colitis. Inflamm Bowel Dis. 2007;13:219–224

 Conflicts of interest The authors disclose no conflicts.

 Funding This work was supported by the National Health and Medical Research Council of Australia, the Cancer Council of Victoria (R.G.R.), National Institutes of Health grant CA32551 (E.R.S.), the Albert Einstein College of Medicine Cancer Center grant 5P30-CA13330, an American Society of Hematology Fellow Scholar Award (X.-M.D.), and a Leukaemia and Lymphoma Society Special Fellow Award (X.-M.D.).

PII: S0016-5085(09)00375-8

doi: 10.1053/j.gastro.2009.03.004

Gastroenterology
Volume 137, Issue 1 , Pages 136-144.e3 , July 2009

Article Tools

* Image Usage & Resolution