Gastrointestinal Stem Cells and Research Progress of Its Role in Gastric Neoplasms_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

WANG Jia , YU Jiwei ,  JIANG Bojian

The First Department of General Surgery， No. 3 People’s Hospital， Shanghai Jiao-tong University School of Medicine， Shanghai 201900， China;

Corresponding author：

JIANG Bojian, Email: jiang_md@hotmail.com

Keywords：

Gastrointestinal stem cell; Gastric neoplasm; Stem cell marker

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective 　To summarize the research progress of gastrointestinal stem cells and its role in gastric neoplasms.
Methods 　The literatures related effect of gastrointestinal stem cells niche， gastrointestinal stem cells markers，
and the cancer stem cell theory in the gastric neoplasms were retrieved through PubMed， the research progress of gastrointestinal stem cells and cancer stem cells in the gastric neoplasms was explored.
Results 　The cancer stem cell theory arose a decade ago. Gastrointestinal stem cells played a very important role in the gastric neoplasms， which had specific markers and their niches included many kinds of tissue factors. Inflammation could induce gastrointestinal stem cells dysplasia and become cancer stem cells， which promoted the growth， invasion， and metastasis of the gastric neoplasms.
Conclusions 　Gastric cancer stem cells could be one of an effective target in treatment for gastric neoplasms， and it may be provide a new breakthrough in treatment for gastric neoplasms.

Citation： WANG Jia,YU Jiwei,JIANG Bojian,.. Gastrointestinal Stem Cells and Research Progress of Its Role in Gastric Neoplasms. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2013, 20(2): 221-226. doi: Copy

1.	van der Flier LG， van Gijn ME， Hatzis P， et al. Transcription factor achaete scute-like 2 controls intestinal stem cell fate[J]. Cell， 2009， 136(5)：903-912.
2.	McNairn AJ， Guasch G. Epithelial transition zones：mergingmicroenvironments， niches， and cellular transformation[J]. Eur J Dermatol， 2011， 21 Suppl 2：21-28.
3.	Levin DE， Grikscheit TC. Tissue-engineering of the gastrointestinal tract[J]. Curr Opin Pediatr， 2012， 24(3)：365-370.
4.	Haegebarth A， Clevers H. Wnt signaling， Lgr5， and stem cells in the intestine and skin[J]. Am J Pathol， 2009， 174(3)：715-721.
5.	Neal MD， Richardson WM， Sodhi CP， et al. Intestinal stem cells and their roles during mucosal injury and repair[J]. J Surg Res， 2011， 167(1)：1-8.
6.	Sato T， Vries RG， Snippert HJ， et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche[J]. Nature， 2009， 459(7244)：262-265.
7.	Sato T， van Es JH， Snippert HJ， et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts[J]. Nature， 2011， 469(7330)：415-418.
8.	Kim TH， Escudero S， Shivdasani RA. Intact function of Lgr5 receptor-expressing intestinal stem cells in the absence of Paneth cells[J]. Proc Natl Acad Sci USA， 2012， 109(10)：3932-3937.
9.	Saikawa Y， Fukuda K， Takahashi T， et al. Gastric carcinogenesis and the cancer stem cell hypothesis[J]. Gastric Cancer， 2010， 13(1)：11-24.
10.	Karam SM. A focus on parietal cells as a renewing cell population[J]. World J Gastroenterol， 2010， 16(5)：538-546.
11.	Bredemeyer AJ， Geahlen JH， Weis VG， et al. The gastric epithelialprogenitor cell niche and differentiation of the zymogenic (chief) cell lineage[J]. Dev Biol， 2009， 325(1)：211-224.
12.	Nam KT， Lee HJ， Sousa JF， et al. Mature chief cells are cryptic progenitors for metaplasia in the stomach[J]. Gastroenterology， 2010， 139(6)：2028-2037.
13.	Goldenring JR， Nam KT， Mills JC. The origin of pre-neoplastic metaplasia in the stomach：chief cells emerge from the Mist[J]. Exp Cell Res， 2011， 317(19)：2759-2764.
14.	Qiao XT， Gumucio DL. Current molecular markers for gastric progenitor cells and gastric cancer stem cells[J]. J Gastroenterol， 2011， 46(7)：855-865.
15.	Barker N， Huch M， Kujala P， et al. Lgr5+ve stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro[J]. Cell Stem Cell， 2010， 6(1)：25-36.
16.	Fan XS， Wu HY， Yu HP， et al. Expression of Lgr5 in human colorectal carcinogenesis and its potential correlation with beta-catenin[J]. Int J Colorectal Dis， 2010， 25(5)：583-590.
17.	Leushacke M， Barker N. Lgr5 and Lgr6 as markers to study adult stem cell roles in self-renewal and cancer[J]. Oncogene， 2012， 31(25)：3009-3022.
18.	Simon E， Petke D， Böger C， et al. The spatial distribution of LGR5+ cells correlates with gastric cancer progression[J]. PLoS One， 2012， 7(4)：e35486.
19.	Quante M， Marrache F， Goldenring JR， et al. TFF2 mRNA transcript expression marks a gland progenitor cell of the gastric oxyntic mucosa[J]. Gastroenterology， 2010， 139(6)：2018-2027.
20.	Huh WJ， Esen E， Geahlen JH， et al. XBP1 controls maturation of gastric zymogenic cells by induction of MIST1 and expansion of the rough endoplasmic reticulum[J]. Gastroenterology， 2010， 139(6)：2038-2049.
21.	Tian X， Jin RU， Bredemeyer AJ， et al. RAB26 and RAB3D are direct transcriptional targets of MIST1 that regulate exocrine granulematuration[J]. Mol Cell Biol， 2010， 30(5)：1269-1284.
22.	Lennerz JK， Kim SH， Oates EL， et al. The transcription factor MIST1 is a novel human gastric chief cell marker whose expression is lost in metaplasia， dysplasia， and carcinoma[J]. Am J Pathol， 2010， 177(3)：1514-1533.
23.	Zhang Y， Huang X. Investigation of doublecortin and calcium/calmodulin-dependent protein kinase-like-1-expressing cells in the mouse stomach[J]. J Gastroenterol Hepatol， 2010， 25(3)：576-582.
24.	Kikuchi M， Nagata H， Watanabe N， et al. Altered expression of a putative progenitor cell marker DCAMKL1 in the rat gastric mucosa in regeneration， metaplasia and dysplasia[J]. BMC Gastroenterol， 2010， 10：65.
25.	Snippert HJ， van Es JH， van den Born M， et al. Prominin-1/CD133 marks stem cells and early progenitors in mouse smallintestine[J]. Gastroenterology， 2009， 136(7)：2187-2194.
26.	Zhu L， Gibson P， Currle DS， et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation[J]. Nature， 2009， 457(7229)：603-607.
27.	Fukamachi H， Shimada S， Ito K， et al. CD133 is a marker of gland-forming cells in gastric tumors and Sox17 is involved in its regulation[J]. Cancer Sci， 2011， 102(7)：1313-1321.
28.	Cao L， Hu X， Zhang Y， et al. Omental milky spots in screening gastric cancer stem cells[J]. Neoplasma， 2011， 58(1)：20-26.
29.	Yasui W， Sentani K， Sakamoto N， et al. Molecular pathology of gastric cancer：research and practice[J]. Pathol Res Pract， 2011， 207(10)：608-612.
30.	Matkar SS， Durham A， Brice A， et al. Systemic activation of K-ras rapidly induces gastric hyperplasia and metaplasia in mice[J]. Am J Cancer Res， 2011， 1(4)：432-445.
31.	da Cunha CB， Oliveira C， Wen X， et al. De novo expression of CD44 variants in sporadic and hereditary gastric cancer[J]. Lab Invest， 2010， 90(11)：1604-1614.
32.	Palagani V， El Khatib M， Krech T， et al. Decrease of CD44-positive cells correlates with tumor response to chemotherapy in patients with gastrointestinal cancer[J]. Anticancer Res， 2012， 32(5)：1747-1755.
33.	Takaishi S， Okumura T， Tu S， et al. Identification of gastric cancer stem cells using the cell surface marker CD44[J]. Stem Cells， 2009， 27(5)：1006-1020.
34.	Dhingra S， Feng W， Brown RE， et al. Clinicopathologic significance of putative stem cell markers， CD44 and nestin， in gastric adenocarcinoma[J]. Int J Clin Exp Pathol， 2011， 4(8)：733-741.
35.	Arnold K， Sarkar A， Yram MA， et al. Sox2+ adult stem andprogenitor cells are important for tissue regeneration and survival of mice[J]. Cell Stem Cell， 2011， 9(4)：317-329.
36.	Honda A， Hirose M， Hatori M， et al. Generation of induced pluripotent stem cells in rabbits：potential experimental models for human regenerative medicine[J]. J Biol Chem， 2010， 285(41)：31362-31369.
37.	Kirchner T， Muller S， Hattori T， et al. Metaplasia， intraepithelialneoplasia and early cancer of the stomach are related to dedifferentiated epithelial cells defined by cytokeratin-7 expression in gastritis[J]. Virchows Arch， 2001， 439(4)：512-522.
38.	Karam SM. Mouse models demonstrating the role of stem/progenitor cells in gastric carcinogenesis[J]. Front Biosci， 2010， 15：595-603.
39.	Houghton J， Stoicov C， Nomura S， et al. Gastric cancer originating from bone marrowderived cells[J]. Science， 2004， 306(5701)：1568-1571.
40.	Quante M， Tu SP， Tomita H， et al. Bone marrow-derivedmyofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth[J]. Cancer Cell， 2011， 19(2)：257-272.
41.	Shibata W， Ariyama H， Westphalen CB， et al. Stromal cell-derived factor-1 overexpression induces gastric dysplasia through expansion of stromal myofibroblasts and epithelial progenitors[J]. Gut， 2012 Feb 23. [Epub ahead of print].
42.	Pilpilidis I， Kountouras J， Zavos C， et al. Upper gastrointestinal carcinogenesis：H. pylori and stem cell cross-talk[J]. J Surg Res， 2011， 166(2)：255-264.
43.	Varon C， Dubus P， Mazurier F， et al. Helicobacter pylori infectionrecruits bone marrow-derived cells that participate in gastric prene-oplasia in mice[J]. Gastroenterology， 2012， 142(2)：281-291.
44.	Kouznetsova I， Kalinski T， Meyer F， et al. Self-renewal of the human gastric epithelium：new insights from expression profiling using laser microdissection[J]. Mol Biosyst， 2011， 7(4)：1105-1112.
45.	Polk DB， Peek RM Jr. Helicobacter pylori：gastric cancer and beyond[J]. Nat Rev Cancer， 2010， 10(6)：403-414.
46.	Ding SZ， Goldberg JB， Hatakeyama M. Helicobacter pyloriinfection， oncogenic pathways and epigenetic mechanisms in gastriccarcinogenesis[J]. Future Oncol， 2010， 6(5)：851-862.
47.	Seoane J. NO signals from the cancer stem cell niche[J]. Cell Stem Cell， 2010， 6(2)：97-98.
48.	Takebe N， Harris PJ， Warren RQ， et al. Targeting cancer stem cells by inhibiting Wnt， Notch， and Hedgehog pathways[J]. Nat Rev Clin Oncol， 2011， 8(2)：97-106.
49.	Takebe N， Ivy SP. Controversies in cancer stem cells：targetingembryonic signaling pathways[J]. Clin Cancer Res， 2010， 16(12)：3106-3112.
50.	Martelli AM， Evangelisti C， Follo MY， et al. Targeting the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin signaling network in cancer stem cells[J]. Curr Med Chem， 2011， 18(18)：2715-2726.
51.	Thiel A， Mrena J， Ristimäki A. Cyclooxygenase-2 and gastric cancer[J]. Cancer Metastasis Rev， 2011， 30(3-4)：387-395.
52.	Futagami S， Hamamoto T， Shimpuku M， et al. Celecoxib inhibitsCD133-positive cell migration via reduction of CCR2 in Helicobacter pylori-infected Mongolian gerbils[J]. Digestion， 2010， 81(3)：193-203.
53.	Stoicov C， Li H， Cerny J， et al. How the study of Helicobacter infection can contribute to the understanding of carcinoma development[J]. Clin Microbiol Infect， 2009， 15(9)：813-822.
54.	Cukierman E， Bassi DE. The mesenchymal tumor microenvironment：a drug-resistant niche[J]. Cell Adh Migr， 2012， 6(3)：285-296.
55.	Cabarcas SM， Mathews LA， Farrar WL. The cancer stem cell niche-there goes the neighborhood?[J]. Int J Cancer， 2011， 129(10)：2315-2327.

1. van der Flier LG， van Gijn ME， Hatzis P， et al. Transcription factor achaete scute-like 2 controls intestinal stem cell fate[J]. Cell， 2009， 136(5)：903-912.
2. McNairn AJ， Guasch G. Epithelial transition zones：mergingmicroenvironments， niches， and cellular transformation[J]. Eur J Dermatol， 2011， 21 Suppl 2：21-28.
3. Levin DE， Grikscheit TC. Tissue-engineering of the gastrointestinal tract[J]. Curr Opin Pediatr， 2012， 24(3)：365-370.
4. Haegebarth A， Clevers H. Wnt signaling， Lgr5， and stem cells in the intestine and skin[J]. Am J Pathol， 2009， 174(3)：715-721.
5. Neal MD， Richardson WM， Sodhi CP， et al. Intestinal stem cells and their roles during mucosal injury and repair[J]. J Surg Res， 2011， 167(1)：1-8.
6. Sato T， Vries RG， Snippert HJ， et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche[J]. Nature， 2009， 459(7244)：262-265.
7. Sato T， van Es JH， Snippert HJ， et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts[J]. Nature， 2011， 469(7330)：415-418.
8. Kim TH， Escudero S， Shivdasani RA. Intact function of Lgr5 receptor-expressing intestinal stem cells in the absence of Paneth cells[J]. Proc Natl Acad Sci USA， 2012， 109(10)：3932-3937.
9. Saikawa Y， Fukuda K， Takahashi T， et al. Gastric carcinogenesis and the cancer stem cell hypothesis[J]. Gastric Cancer， 2010， 13(1)：11-24.
10. Karam SM. A focus on parietal cells as a renewing cell population[J]. World J Gastroenterol， 2010， 16(5)：538-546.
11. Bredemeyer AJ， Geahlen JH， Weis VG， et al. The gastric epithelialprogenitor cell niche and differentiation of the zymogenic (chief) cell lineage[J]. Dev Biol， 2009， 325(1)：211-224.
12. Nam KT， Lee HJ， Sousa JF， et al. Mature chief cells are cryptic progenitors for metaplasia in the stomach[J]. Gastroenterology， 2010， 139(6)：2028-2037.
13. Goldenring JR， Nam KT， Mills JC. The origin of pre-neoplastic metaplasia in the stomach：chief cells emerge from the Mist[J]. Exp Cell Res， 2011， 317(19)：2759-2764.
14. Qiao XT， Gumucio DL. Current molecular markers for gastric progenitor cells and gastric cancer stem cells[J]. J Gastroenterol， 2011， 46(7)：855-865.
15. Barker N， Huch M， Kujala P， et al. Lgr5+ve stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro[J]. Cell Stem Cell， 2010， 6(1)：25-36.
16. Fan XS， Wu HY， Yu HP， et al. Expression of Lgr5 in human colorectal carcinogenesis and its potential correlation with beta-catenin[J]. Int J Colorectal Dis， 2010， 25(5)：583-590.
17. Leushacke M， Barker N. Lgr5 and Lgr6 as markers to study adult stem cell roles in self-renewal and cancer[J]. Oncogene， 2012， 31(25)：3009-3022.
18. Simon E， Petke D， Böger C， et al. The spatial distribution of LGR5+ cells correlates with gastric cancer progression[J]. PLoS One， 2012， 7(4)：e35486.
19. Quante M， Marrache F， Goldenring JR， et al. TFF2 mRNA transcript expression marks a gland progenitor cell of the gastric oxyntic mucosa[J]. Gastroenterology， 2010， 139(6)：2018-2027.
20. Huh WJ， Esen E， Geahlen JH， et al. XBP1 controls maturation of gastric zymogenic cells by induction of MIST1 and expansion of the rough endoplasmic reticulum[J]. Gastroenterology， 2010， 139(6)：2038-2049.
21. Tian X， Jin RU， Bredemeyer AJ， et al. RAB26 and RAB3D are direct transcriptional targets of MIST1 that regulate exocrine granulematuration[J]. Mol Cell Biol， 2010， 30(5)：1269-1284.
22. Lennerz JK， Kim SH， Oates EL， et al. The transcription factor MIST1 is a novel human gastric chief cell marker whose expression is lost in metaplasia， dysplasia， and carcinoma[J]. Am J Pathol， 2010， 177(3)：1514-1533.
23. Zhang Y， Huang X. Investigation of doublecortin and calcium/calmodulin-dependent protein kinase-like-1-expressing cells in the mouse stomach[J]. J Gastroenterol Hepatol， 2010， 25(3)：576-582.
24. Kikuchi M， Nagata H， Watanabe N， et al. Altered expression of a putative progenitor cell marker DCAMKL1 in the rat gastric mucosa in regeneration， metaplasia and dysplasia[J]. BMC Gastroenterol， 2010， 10：65.
25. Snippert HJ， van Es JH， van den Born M， et al. Prominin-1/CD133 marks stem cells and early progenitors in mouse smallintestine[J]. Gastroenterology， 2009， 136(7)：2187-2194.
26. Zhu L， Gibson P， Currle DS， et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation[J]. Nature， 2009， 457(7229)：603-607.
27. Fukamachi H， Shimada S， Ito K， et al. CD133 is a marker of gland-forming cells in gastric tumors and Sox17 is involved in its regulation[J]. Cancer Sci， 2011， 102(7)：1313-1321.
28. Cao L， Hu X， Zhang Y， et al. Omental milky spots in screening gastric cancer stem cells[J]. Neoplasma， 2011， 58(1)：20-26.
29. Yasui W， Sentani K， Sakamoto N， et al. Molecular pathology of gastric cancer：research and practice[J]. Pathol Res Pract， 2011， 207(10)：608-612.
30. Matkar SS， Durham A， Brice A， et al. Systemic activation of K-ras rapidly induces gastric hyperplasia and metaplasia in mice[J]. Am J Cancer Res， 2011， 1(4)：432-445.
31. da Cunha CB， Oliveira C， Wen X， et al. De novo expression of CD44 variants in sporadic and hereditary gastric cancer[J]. Lab Invest， 2010， 90(11)：1604-1614.
32. Palagani V， El Khatib M， Krech T， et al. Decrease of CD44-positive cells correlates with tumor response to chemotherapy in patients with gastrointestinal cancer[J]. Anticancer Res， 2012， 32(5)：1747-1755.
33. Takaishi S， Okumura T， Tu S， et al. Identification of gastric cancer stem cells using the cell surface marker CD44[J]. Stem Cells， 2009， 27(5)：1006-1020.
34. Dhingra S， Feng W， Brown RE， et al. Clinicopathologic significance of putative stem cell markers， CD44 and nestin， in gastric adenocarcinoma[J]. Int J Clin Exp Pathol， 2011， 4(8)：733-741.
35. Arnold K， Sarkar A， Yram MA， et al. Sox2+ adult stem andprogenitor cells are important for tissue regeneration and survival of mice[J]. Cell Stem Cell， 2011， 9(4)：317-329.
36. Honda A， Hirose M， Hatori M， et al. Generation of induced pluripotent stem cells in rabbits：potential experimental models for human regenerative medicine[J]. J Biol Chem， 2010， 285(41)：31362-31369.
37. Kirchner T， Muller S， Hattori T， et al. Metaplasia， intraepithelialneoplasia and early cancer of the stomach are related to dedifferentiated epithelial cells defined by cytokeratin-7 expression in gastritis[J]. Virchows Arch， 2001， 439(4)：512-522.
38. Karam SM. Mouse models demonstrating the role of stem/progenitor cells in gastric carcinogenesis[J]. Front Biosci， 2010， 15：595-603.
39. Houghton J， Stoicov C， Nomura S， et al. Gastric cancer originating from bone marrowderived cells[J]. Science， 2004， 306(5701)：1568-1571.
40. Quante M， Tu SP， Tomita H， et al. Bone marrow-derivedmyofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth[J]. Cancer Cell， 2011， 19(2)：257-272.
41. Shibata W， Ariyama H， Westphalen CB， et al. Stromal cell-derived factor-1 overexpression induces gastric dysplasia through expansion of stromal myofibroblasts and epithelial progenitors[J]. Gut， 2012 Feb 23. [Epub ahead of print].
42. Pilpilidis I， Kountouras J， Zavos C， et al. Upper gastrointestinal carcinogenesis：H. pylori and stem cell cross-talk[J]. J Surg Res， 2011， 166(2)：255-264.
43. Varon C， Dubus P， Mazurier F， et al. Helicobacter pylori infectionrecruits bone marrow-derived cells that participate in gastric prene-oplasia in mice[J]. Gastroenterology， 2012， 142(2)：281-291.
44. Kouznetsova I， Kalinski T， Meyer F， et al. Self-renewal of the human gastric epithelium：new insights from expression profiling using laser microdissection[J]. Mol Biosyst， 2011， 7(4)：1105-1112.
45. Polk DB， Peek RM Jr. Helicobacter pylori：gastric cancer and beyond[J]. Nat Rev Cancer， 2010， 10(6)：403-414.
46. Ding SZ， Goldberg JB， Hatakeyama M. Helicobacter pyloriinfection， oncogenic pathways and epigenetic mechanisms in gastriccarcinogenesis[J]. Future Oncol， 2010， 6(5)：851-862.
47. Seoane J. NO signals from the cancer stem cell niche[J]. Cell Stem Cell， 2010， 6(2)：97-98.
48. Takebe N， Harris PJ， Warren RQ， et al. Targeting cancer stem cells by inhibiting Wnt， Notch， and Hedgehog pathways[J]. Nat Rev Clin Oncol， 2011， 8(2)：97-106.
49. Takebe N， Ivy SP. Controversies in cancer stem cells：targetingembryonic signaling pathways[J]. Clin Cancer Res， 2010， 16(12)：3106-3112.
50. Martelli AM， Evangelisti C， Follo MY， et al. Targeting the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin signaling network in cancer stem cells[J]. Curr Med Chem， 2011， 18(18)：2715-2726.
51. Thiel A， Mrena J， Ristimäki A. Cyclooxygenase-2 and gastric cancer[J]. Cancer Metastasis Rev， 2011， 30(3-4)：387-395.
52. Futagami S， Hamamoto T， Shimpuku M， et al. Celecoxib inhibitsCD133-positive cell migration via reduction of CCR2 in Helicobacter pylori-infected Mongolian gerbils[J]. Digestion， 2010， 81(3)：193-203.
53. Stoicov C， Li H， Cerny J， et al. How the study of Helicobacter infection can contribute to the understanding of carcinoma development[J]. Clin Microbiol Infect， 2009， 15(9)：813-822.
54. Cukierman E， Bassi DE. The mesenchymal tumor microenvironment：a drug-resistant niche[J]. Cell Adh Migr， 2012， 6(3)：285-296.
55. Cabarcas SM， Mathews LA， Farrar WL. The cancer stem cell niche-there goes the neighborhood?[J]. Int J Cancer， 2011， 129(10)：2315-2327.

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Gastrointestinal Stem Cells and Research Progress of Its Role in Gastric Neoplasms

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