Concise review: Adult salivary gland stem cells and a potential therapy for xerostomia

Stem Cells

Volumn 31, Issue 4, 2013, Pages 613-619

  Pringle, Sarah ^a   Van Os, Ronald ^a   Coppes, Robert P ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Cellular therapy; Hyposalivation; Regeneration; Stem progenitor cells

Indexed keywords

ALPHA6 INTEGRIN; BETA1 INTEGRIN; CD24 ANTIGEN; HYALURONIDASE; STEM CELL FACTOR RECEPTOR;

ACINAR CELL; CANCER RADIOTHERAPY; CELL POPULATION; CELL PROLIFERATION; CULTURE OPTIMIZATION; GOOD MANUFACTURING PRACTICE; HEAD AND NECK CANCER; HUMAN; HYPOSALIVATION; LONG TERM CARE; NONHUMAN; PROTEIN EXPRESSION; QUALITY OF LIFE; RADIATION STERILIZATION; REVIEW; SALIVARY GLAND; SALIVATION; STEM CELL TRANSPLANTATION; SYMPTOM; XEROSTOMIA;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; SALIVARY GLANDS; STEM CELL TRANSPLANTATION; TISSUE THERAPY; XEROSTOMIA;

EID: 84875786405     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1327     Document Type: Review

References (81)

1. American Cancer Society Cancer Facts and Figures 2012. Atlanta: American Cancer Society, 2012, Available at: http://www.cancer.org/research/ cancerfactsfigures/cancerfactsfigures/cancer-facts-figures-2012.
2. Piccirillo JF, Costas I, Reichman ME. Cancers of the head and neck. In: Ries LAG, Young JL, Keel GE et al., eds. SEER Survival Monograph: Cancer Survival Among Adults: U.S. SEER Program, 1988-2001, Patient and Tumor Characteristics. 1st ed. Bethesda, MD: National Cancer Institute, 2007;7-22.
3. Burlage FR, Coppes RP, Meertens H et al. Parotid and submandibular/ sublingual salivary flow during high dose radiotherapy. Radiother Oncol 2001;61:271-274.
4. Jansma J, Vissink A, Spijkervet FK et al. Protocol for the prevention and treatment of oral sequelae resulting from head and neck radiation therapy. Cancer 1992;70:2171-2180.
5. Jellema AP, Slotman BJ, Doornaert P et al. Impact of radiationinduced xerostomia on quality of life after primary radiotherapy among patients with head and neck cancer. Int J Radiat Oncol Biol Phys 2007;69:751-760.
6. Malouf JG, Aragon C, Henson BS et al. Influence of parotid-sparing radiotherapy on xerostomia in head and neck cancer patients. Cancer Detect Prev 2003;27:305-310.
7. Vergeer MR, Doornaert PAH, Rietveld DHF et al. Intensity-modulated radiotherapy reduces radiation-induced morbidity and improves health-related quality of life: Results of a nonrandomized prospective study using a standardized follow-up program. Int J Radiat Oncol Biol Phys 2009;74:1-8.
8. Vissink A, Burlage FR, Spijkervet FKL et al. Prevention and treatment of the consequences of head and neck radiotherapy. Crit Rev Oral Biol Med 2003;14:213-225.
9. Vissink A, Jansma J, Spijkervet FKL et al. Oral sequelae of head and neck radiotherapy. Crit Rev Oral Biol Med 2003;14: 199-212.
10. Pavlov IP. The scientific investigation of the psychical faculties or processes in the higher animals. Science 1906;24:613-619.
11. Proctor GB, Carpenter GH. Regulation of salivary gland function by autonomic nerves. Auton Neurosci 2007;133:3-18.
12. Sreebny LM. The causes of dry mouth: A broad panoply. In: Sreebny LM, Vissink A, eds. Dry Mouth the Malevolent Symptom: A Clinical Guide. 1st ed. Iowa, IA: Blackwell Publishing, 2010;139-151.
13. Coppes RP, Zeilstra LJW, Kampinga HH et al. Early to late sparing of radiation damage to the parotid gland by adrenergic and muscarinic receptor agonists. Br J Cancer 2001;85:1055-1063.
14. Konings AWT, Coppes RP, Vissink A. On the mechanism of salivary gland radiosensitivity. Int J Radiat Oncol Biol Phys 2005;62: 1187-1194.
15. Abok K, Brunk U, Jung B et al. Morphologic and histochemical studies on the differing radiosensitivity of ductular and acinar cells of the rat submandibular gland. Virchows Arch B Cell Pathol Incl Mol Pathol 1984;45:443-460.
16. Nagler R, Marmary Y, Fox PC et al. Irradiation-induced damage to the salivary glands: The role of redox-active iron and copper. Radiat Res 1997;147:468-476.
17. Zeilstra LJW, Vissink A, Konings AWT et al. Radiation induced cell loss in rat submandibular gland and its relation to gland function. Int J Radiat Biol 2000;76:419-429.
18. Stephens CL, Schultheiss TE, Price RE et al. Radiation apoptosis of serous acinar cells of salivary and lacrimal glands. Cancer 1991;67: 1539-1543.
19. Stephens CL, Schultheiss TE, Small SM et al. Response of parotid gland organ culture to radiation. Radiat Res 1989;120: 140-153.
20. Denny PC, Denny PA. Dynamics of parenchymal cell division, differentiation and apoptosis in the young adult female mouse submandibular gland. Anat Rec 1999;254:408-417.
21. Denny PC, Chai Y, Klauser DK et al. Parenchymal cell proliferation and mechanisms for maintenance of granular duct and acinar cell populations in adult male mouse submandibular gland. Anat Rec 2005;235:475-485.
22. Man YG, Ball WD, Marchetti L et al. Contributions of intercalated duct cells to the normal parenchyma of submandibular glands of adult rats. Anat Rec 2001;263:202-214.
23. Konings AWT, Faber H, Cotteleer F et al. Secondary radiation damage as the main cause for unexpected volume effects: A histopathologic study of the parotid gland. Int J Radiat Oncol Biol Phys 2006;64:98-105.
24. Ihrler S, Zietz C, Sendelhofert A et al. A morphogenetic concept of salivary duct regeneration and metaplasia. Virchows Arch 2002;440: 519-526.
25. Roesink JM, Konings AWT, Terhaard CHJ et al. Preservation of the rat parotid gland function after radiation by prophylactic pilocarpine treatment: Radiation dose dependency and compensatory mechanisms. Int J Radiat Oncol Biol Phys 1999;45:483-489.
26. Liu RP, Fleming TJ, Toth BB et al. Salivary flow rates in patients with head and neck cancer 0.5 to 25 years after radiotherapy. Int J Radiat Oncol Biol Phys 1993;70:724.
27. Shackleton M, Vaillant F, Simpson KJ et al. Generation of a functional mammary gland from a single stem cell. Nature 2006;439: 84-88.
28. Stingl J, Eirew P, Ricketson I et al. Purification and unique properties of mammary epithelial stem cells. Nature 2005;439:993-997.
29. Liao M, Zhang CC, Zhou B et al. Enrichment of a population of mammary gland cells that form mammospheres and have in vivo repopulating activity. Cancer Res 2007;67:8131-8138.
30. Reynolds B, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-1710.
31. Garraway IP, Sun W, Tran CP et al. Human prostate sphere-forming cells represent a subset of basal epithelial cells capable of glandular regeneration in vivo. Prostate 2010;70:491-501.
32. Collins AT, Habib FK, Maitland NJ et al. Identification and isolation of human prostate epithelial stem cells based on a2b1-integrin expression. J Cell Sci 2001;114:3865-3872.
33. 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.
34. Braam PM, Roesink JM, Moerland MA et al. Long-term parotid gland function after radiotherapy. Int J Radiat Oncol Biol Phys 2005;62: 659-664.
35. Takahashi S, Nakamura S, Shinazato K et al. Apoptosis and proliferation of myoepithelial cells in atrophic rat submandibular glands. J Histochem Cytochem 2001;49:1557-1564.
36. Osailan SM, Proctor GB, McGurk M et al. Intraoral duct ligation without inclusion of the parasympatheticnerve supply induces rat submandibular gland atrophy. Int J Exp Pathol 2006;87: 41-48.
37. Cotroneo E, Proctor GB, Paterson KL et al. Early markers of regeneration following ductal ligation in rat submandibular gland. Cell Tissue Res 2008;332:227-235.
38. Cotroneo E, Proctor GB, Carpenter GH. Regeneration of acinar cells following ligation of rat submandibular gland retraces the embryonicperinatal pathway of cytodifferentiation. Differentiation 2010;79: 120-130.
39. Man YG, Ball WD, Culp DJ et al. Persistence of a perinatal cellular phenotype in submandibular glands of adult rat. J Histochem Cytochem 1995;43:1203-1215.
40. Takahashi S, Shinzato K, Domon T et al. Mitotic proliferation of myoepithelial cells during regeneration of atrophied rat submandibular glands after duct ligation. J Oral Pathol Med 2004;33:430-434.
41. Katsumata O, Yu-Ichi Sato Y, Sakai Y et al. Intercalated duct cells in the rat parotid gland maybehave as tissue stem cells. Anat Sci Int 2009;84:148-154.
42. Lombaert IM, Wierenga PK, Kok T et al. Mobilization of bone marrow stem cells by granulocyte colony-stimulating factor ameliorates radiation-induced damage to salivary glands. Clin Cancer Res 2006; 12:1804-1812.
43. Lombaert IM, Brunsting JF, Wierenga PK et al. Keratinocyte growth factor prevents radiation damage to salivary glands by expansion of the stem/progenitor pool. Stem Cells 2008;26: 2595-2601.
44. Lombaert IM, Brunsting JF, Wierenga PK et al. Rescue of salivary gland function after stem cell transplantation in irradiated glands. PLoS One 2008;3:e2063.
45. Nanduri LSY, Maimets M, Pringle SA et al. Regeneration of irradiated salivary glands with stem cell marker expressing cells. Radiother Oncol 2011;99:367-372.
46. Banh A, Xiao N, Cao H et al. A novel aldehyde dehydrogenase-3 activator leads to adult salivary stem cell enrichment in vivo. Clin Cancer Res 2011;17:7265-7272.
47. Mishima K, Inoue H, Nishiyama T et al. Transplantation of side population cells restores the function of damaged exocrine glands through clusterin. Stem Cells 2012;30:1925-1937.
48. Rugel-Stahl A, Elliott ME, Ovitt CE Ascl3 marks adult progenitor cells of the mouse salivary gland. Stem Cell Res 2012;8: 379-387.
49. Kishi T, Takao T, Fujita K et al. Clonal proliferation of multipotent stem/progenitor cells in the neonatal and adult salivary glands. Biochem Biophys Res Commun 2006;340:544-552.
50. David R, Shai E, Aframian DJ et al. Isolation and cultivation of integrin a6b1-expressing salivary gland graft cells: A model for use with an artificial salivary gland. Tissue Eng Part A 2008;14: 331-337.
51. Neumann Y, David R, Stiubea-Cohen R et al. Long-term cryopreservation model of rat salivary gland stem cells for future therapy in irradiated head and neck cancer patients. Tissue Eng Part C 2012;18: 710-718.
52. Sato A, Okumura K, Matsumoto S et al. Isolation, tissue localization, and cellular characterization of progenitors derived from adult human salivary glands. Cloning Stem Cells 2007;9:191-205.
53. Feng J, van der Zwaag M, Stokman MA et al. Isolation and characterization of human salivary gland cells for stem cell transplantation to reduce radiation-induced hyposalivation. Radiother Oncol 2009;92: 466-471.
54. Maria O, Maria A, Cai Y et al. Cell surface markers CD44 and CD166 localized specific populations of salivary acinar cells. Oral Dis 2012;18:162-168.
55. Palmon A, David R, Neumann Y et al. High-efficiency immunomagnetic isolation of solid tissue-originated integrin-expressing adult stem cells. Methods 2012;56:305-309.
56. Pringle S, Nanduri LSY, van der Zwaag M et al. Isolation of mouse salivary gland stem cells. J Vis Exp 2011:e2484.
57. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282:1145-1147.
58. Reubinoff BE, Pera MF, Fong CY et al. Embryonic stem cell lines from human blastocysts: Somatic differentiation in vitro. Nat Biotechnol 2000;18:399-404.
59. Alper J. Geron gets green light for human trial of ES cell-derived product. Nat Biotechnol 2009;27:213-214.
60. Baker DEC, Harrison NJ, Maltby E et al. Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol 2007;25:207-215.
61. Hussein SM, Batada NN, Vuoristo S et al. Copy number variation and selection during reprogramming to pluripotency. Nature 2011;471: 58-62.
62. Karamouzian S, Nematollahi-Mahani SN, Nakhaee N et al. Clinical safety and primary efficacy of bone marrow mesenchymal cell transplantation in subacute spinal cord injured patients. Clin Neurol Neurosurg 2012;114:935-939.
63. Tan J, Wu W, Xu X et al. Induction therapy with autologous mesenchymal stem cells in living-related kidney transplants. JAMA 2012; 307:1169-1177.
64. Couzin J. A shot of bone marrow can help the heart. Science 2006; 313:1715-1716.
65. Lagasse E, Connors H, Al-Dhalimy M et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 2000;6: 1229-1234.
66. Nishida M, Fujimoto S, Toiyama K et al. Effect of hematopoietic cytokines on renal function in cisplatin-induced ARF in mice. Biochem Biophys Res Commun 2004;324:341-347.
67. Orlic D, Kajstura J, Chimenti S et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001;410:701.
68. Duffield JS, Park KM, Hsiao LL et al. Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 2005;15:1743-1755.
69. Krause D, Cantley LG. Bone marrow plasticity revisited: Protection or differentiation in the kidney tubule? J Clin Invest 2005; 15:1705-1708.
70. Bai L, Lennon DP, Caplan AI et al. Hepatocyte growth factor mediates mesenchymal stem cell-induced recovery in multiple sclerosis models. Nat Neurosci 2012;15:862-870.
71. Passineau MJ, Zourelias L, Machen L et al. Ultrasound-assisted nonviral gene transfer to the salivary glands. Gene Therapy 2010;17: 1318-1324.
72. Jongerius PH, Joosten F, Hoogen FJA et al. The treatment of drooling by ultrasound-guided intraglandular injections of botulinum toxin type a into the salivary glands. Laryngoscope 2003; 113:107-111.
73. Ben-David U, Mayshar Y, Benvenisty N. Large-scale analysis reveals acquisition of lineage-specific chromosomal aberrations in human adult stem cells. Cell Stem Cell 2011;9:97-102.
74. Beetz I, Schilstra C, van der Schaaf A et al. NTCP models for patient-rated xerostomia and sticky saliva after treatment with intensity modulated radiotherapy for head and neck cancer: The role of dosimetric and clinical factors. Radiother Oncol 2012;105:101-106.
75. Hai B, Yang ZH, Millar SE et al. Wnt/beta-catenin signaling regulates postnatal development and regeneration of the salivary gland. Stem Cells Dev 2010;19:1793-1801.
76. Hai B, Yang Z, Shangguan L et al. Concurrent transient activation of Wnt/b-catenin pathway prevents radiation damage to salivary glands. Int J Radiat Oncol Biol Phys 2012;83:109-116.
77. Dang H, Lin AL, Zhang B et al. Role for notch signaling in salivary acinar cell growth and differentiation. Dev Dyn 2009;238: 724-731.
78. Larderet G, Fortunel NO, Vaigot P et al. Human side population keratinocytes exhibit long-term proliferative potential and a specific gene expression profile and can form a pluristratified epidermis. Stem Cells 2006;24:965-974.
79. Golebiewska A, Brons NHC, Bjerkvig R et al. Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell 2011;8:136-147.
80. Martin J, Helm K, Ruegg P et al. Adult lung side population cells have mesenchymal stem cell potential. Cytotherapy 2008;10: 140-151.
81. Pfister O, Mouquet F, Jain M et al. CD31(-) but not CD31(+) cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 2005;97:52-61.