Research progress in cell therapy and tissue engineering approach to regenerate salivary gland_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

DONG Jiao ,  HUANG Guilin

Department of Oral and Maxillofacial Surgery, Stomatological Hospital, Zunyi Medical University, Zunyi Guizhou, 563000, P.R.China;

Corresponding author：

HUANG Guilin, Email: chaojiehuanghgl@163.com

Keywords：

Salivary gland; organoids; stem cells; cell therapy; tissue engineering

DOI：

10.7507/1002-1892.201611101

Video：

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Objective To review the research progress in cell therapy and tissue engineering approach to regenerate salivary gland so as to provide a theoretical basis for the treatment of salivary hypofunction. Methods The recent literature on cell therapy and tissue engineering for the regeneration of salivary glands was reviewed and summarized. Results It is feasible to repair the salivary function by using various stem cells to repair damaged tissue, or by establishing salivary gland tissueex vivo for salivary gland function restoration and reconstruction. However, the mechanism of three dimensional culturing salivary organoids during organogenesis and function expressing and the potential influence of tissue specific extracellular matrix during this process should be further studied. Conclusion Basic research of cell therapy and salivary tissue engineering should be deeply developed, and a standardized culturing system should be establishedin vitro. In addition, it is of great significance to study thein vivo effects of salivary gland-specific cells, non salivary gland epithelial cells and transplanted gene-transfected stem cells.

Citation： DONG Jiao, HUANG Guilin. Research progress in cell therapy and tissue engineering approach to regenerate salivary gland. Chinese Journal of Reparative and Reconstructive Surgery, 2017, 31(3): 369-373. doi: 10.7507/1002-1892.201611101 Copy

1.	Pringle S, Van Os R, Coppes RP. Adult salivary gland stem cells and a potential therapyfor xerostomia. Stem Cells, 2013, 31(4): 613-619.
2.	Vissink A, van Luijk P, Langendijk JA,et al. Current ideas to reduce or salvage radiation damage to salivary glands. Oral Dis, 2015, 21(1): e1-10.
3.	Li Y, Taylor JM, Ten Haken RK,et al. The impact of dose on parotid salivary recovery in head and neck cancer patients treated with radiation therapy. Int J Radiat Oncol Biol Phys, 2007, 67(3): 660-669.
4.	Lombaert IM, Brunsting JF, Wierenga PK,et al. Rescue of salivary gland function after stem cell transplantation in irradiated glands. PLoS One, 2008, 3(4): e2063.
5.	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(3): 466-471.
6.	Gorjup E, Danner S, Rotter N,et al. Glandular tissue from human pancreas and salivary gland yields similar stem cell populations. Eur J Cell Biol, 2009, 88(7): 409-421.
7.	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(10): 2595-2601.
8.	Tatsuishi Y, Hirota M, Kishi T,et al. Human salivary gland stem/progenitor cells remain dormant even after irradiation. Int J Mol Med, 2009, 24(3): 361-366.
9.	van Luijk P, Pringle S, Deasy JO,et al. Sparing the region of the salivary gland containing stem cells preserves saliva production after radiotherapy for head and neck cancer. Sci Transl Med, 2015, 7(305): 305ra147.
10.	Nanduri LS, Lombaert IM, van der Zwaag M,et al. Salisphere derived c-Kit⁺ cell transplantation restores tissue homeostasis in irradiated salivary gland. Radiother Oncol, 2013, 108(3): 458-463.
11.	Xiao N, Lin Y, Cao H,et al. Neurotrophic factor GDNF promotes survival of salivary stem cells. J Clin Invest, 2014, 124(8): 3364-3377.
12.	Coppes RP, Stokman MA. Stem cells and the repair of radiation-induced salivary gland damage. Oral Dis, 2011, 17(2): 143-153.
13.	Nanduri LS, Maimets M, Pringle SA,et al. Regeneration of irradiated salivary glands with stem cell marker expressing cells. Radiother Oncol, 2011, 99(3): 367-372.
14.	Lu L, Li Y, Du MJ,et al. Characterization of a Self-renewing and Multi-potent Cell Population Isolated from Human Minor Salivary Glands. Sci Rep, 2015, 5: 10106.
15.	Banh A, Xiao N, Cao H,et al. A novel aldehyde dehydrogenase-3 activator leads to adult salivary stem cell enrichmentin vivo. Clin Cancer Res, 2011, 17(23): 7265-7272.
16.	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 Methods, 2012, 18(9): 710-718.
17.	Lim JY, Yi T, Choi JS,et al. Intraglandular transplantation of bone marrow-derived clonal mesenchymal stem cells for amelioration of post-irradiation salivary gland damage. Oral Oncol, 2013, 49(2): 136-143.
18.	Zhang NN, Huang GL, Han QB,et al. Functional regeneration of irradiated salivary glands with human amniotic epithelial cells transplantation. Int J Clin Exp Pathol, 2013, 6(10): 2039-2347.
19.	Tran SD, Liu Y, Xia D,et al. Paracrine effects of bone marrow soup restore organ function, regeneration, and repair in salivary glands damaged by irradiation. PLoS One, 2013, 8(4): e61632.
20.	Zheng C, Cotrim AP, Rowzee A,et al. Prevention of radiation-induced salivary hypofunction following hKGF gene delivery to murine submandibular glands. Clin Cancer Res, 2011, 17(9): 2842-2851.
21.	Hai B, Yang Z, Shangguan L,et al. Concurrent transient activation of Wnt/beta-catenin pathway prevents radiation damage to salivary glands. Int J Radiat Oncol Biol Phys, 2012, 83(1): e109-116.
22.	Garcia-Gallastegui P, Ibarretxe G, GarciaRamirez JJ,et al. DLK1 regulates branching morphogenesis and parasympathetic innervation of salivary glands through inhibition of NOTCH signalling. Biol Cell, 2014, 106(8): 237-253.
23.	Hai B, Qin L, Yang Z,et al. Transient activation of hedgehog pathway rescued irradiation-induced hyposalivation by preserving salivary stem/progenitor cells and parasympathetic innervation. Clin Cancer Res, 2014, 20(1): 140-150.
24.	Kojima T, Kanemaru S, Hirano S,et al. The protective efﬁcacy of basic ﬁbroblast growth factor in radiation-induced salivary gland dysfunction in mice. Laryngoscope, 2011, 121(9): 1870-1875.
25.	Marmary Y, Adar R, Gaska S,et al. Radiation-induced loss of salivary gland function is driven by cellular senescence and prevented by IL6 modulation. Cancer Res, 2016, 76(5): 1170-1180.
26.	Hill G, Headon D, Harris ZI,et al. Pharmacological activation of the EDA/EDAR signaling pathway restores salivary gland function following radiation-induced damage. PLoS One, 2014, 9(11): e112840.
27.	Kawakami M, Ishikawa H, Tachibana T,et al. Functional transplantation of salivary gland cells differentiated from mouse early ES cellsin vitro. Hum Cell, 2013, 26(2): 80-90.
28.	Beauchamp P, Mortitz W, Kelm JM,et al. Development and Characterization of a Scaffold-Free 3D Spheroid Model of Induced Pluripotent Stem Cell-Derived Human Cardiomyocytes. Tissue Eng Part C Methods, 2015, 21(8): 852-861.
29.	Ono H, Obana A, Usami Y,et al. Regenerating salivary glands in the microenvironment of induced pluripotent stem cells. Biomed Res Int, 2015, 2015: 293570.
30.	Eiraku M, Watanabe K, Matsuo-Takasaki M,et al. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell, 2008, 3(5): 519-532.
31.	Lancaster MA, Knoblich JA. Organogenesis in a dish: modeling development and disease using organoid technologies. Science, 2014, 345(6194): 1247125.
32.	王军胜, 黄桂林, 张霓霓, 等. 三维培养条件下胚胎鼠唾液腺上皮细胞的自组装. 中国组织工程研究与临床康复, 2011, 15(40): 7549-7553.
33.	Rookmaaker MB, Schutgens F, Verhaar MC,et al. Development and application of human adult stem or progenitor cell organoids. Nat Rev Nephrol, 2015, 11(9): 546-554.
34.	Jang SI, Ong HL, Gallo A,et al. Establishment of functional acinar-like cultures from human salivary glands. J Dent Res, 2015, 94(2): 304-311.
35.	Okumura K, Shinohara M, Endo F. Capability of tissue stem cells to organize into salivary rudiments. Stem Cells Int, 2012, 2012: 502136.
36.	Sneddon JB, Borowiak M, Melton DA. Self-renewal of embryonic-stem-cell-derived progenitors by organ-matched mesenchyme. Nature, 2012, 491(7426): 765-768.
37.	Skardal A, Smith L, Bharadwaj S,et al. Tissue specific synthetic ECM hydrogels for 3Din vitro maintenance of hepatocyte function. Biomaterials, 2012, 33(18): 4565-4575.
38.	Cantara SI, Soscia DA, Sequeira SJ,et al. Selective functionalization of nanofiber scaffolds to regulate salivary gland epithelial cell proliferation and polarity. Biomaterials, 2012, 33(33): 8372-8382.
39.	Pradhan S, Liu C, Zhang C,et al. Lumen formation in three-dimensional cultures of salivary acinar cells. Otolaryngol Head Neck Surg, 2010, 142(2): 191-195.
40.	Yang TL, Hsiao YC. Chitosan facilitates structure formation of the salivary gland by regulating the basement membrane components. Biomaterials, 2015, 66: 29-40.
41.	Maria OM, Maria O, Liu Y,et al. Matrigel improves functional properties of human submandibular salivary gland cell line. Int J Biochem Cell Biol, 2011, 43(4): 622-631.
42.	Gao Z, Wu T, Xu J,et al. Generation of bioartiﬁcial salivary gland using whole-organ decellularized bioscaffold. Cells Tissues Organs, 2014, 200(3-4): 171-180.
43.	Soscia DA, Sequeira SJ, Schramm RA,et al. Salivary gland cell differentiation and organization on micropatterned PLGA nanofiber craters. Biomaterials, 2013, 34(28): 6773-6784.
44.	Peters SB, Naim N, Nelson DA,et al. Biocompatible tissue scaffold compliance promotes salivary gland morphogenesis and differentiation. Tissue Eng Part A, 2014, 20(11-12): 1632-1642.
45.	Daley WP, Gervais EM, Centanni SW,et al. ROCK1-directed basement membrane positioning coordinates epithelial tissue polarity. Development, 2012, 139(2): 411-422.
46.	Cosson S, Allazetta S, Lutolf M P,et al. Patterning of cell-instructive hydrogels by hydrodynamic flow focusing. Lab Chip, 2013, 13(11): 2099-2105.
47.	Zheng Y, Chen J, Craven M,et al.In vitro microvessels for the study of angiogenesis and thrombosis. Proc Natl Acad Sci U S A, 2012, 109(24): 9342-9347.
48.	Pringle S, Maimets M, van der Zwaag M,et al. Human salivary gland stem cells functionally restore radiation damaged salivary glands. Stem Cells, 2016, 34(3): 640-652.

1. Pringle S, Van Os R, Coppes RP. Adult salivary gland stem cells and a potential therapyfor xerostomia. Stem Cells, 2013, 31(4): 613-619.
2. Vissink A, van Luijk P, Langendijk JA,et al. Current ideas to reduce or salvage radiation damage to salivary glands. Oral Dis, 2015, 21(1): e1-10.
3. Li Y, Taylor JM, Ten Haken RK,et al. The impact of dose on parotid salivary recovery in head and neck cancer patients treated with radiation therapy. Int J Radiat Oncol Biol Phys, 2007, 67(3): 660-669.
4. Lombaert IM, Brunsting JF, Wierenga PK,et al. Rescue of salivary gland function after stem cell transplantation in irradiated glands. PLoS One, 2008, 3(4): e2063.
5. 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(3): 466-471.
6. Gorjup E, Danner S, Rotter N,et al. Glandular tissue from human pancreas and salivary gland yields similar stem cell populations. Eur J Cell Biol, 2009, 88(7): 409-421.
7. 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(10): 2595-2601.
8. Tatsuishi Y, Hirota M, Kishi T,et al. Human salivary gland stem/progenitor cells remain dormant even after irradiation. Int J Mol Med, 2009, 24(3): 361-366.
9. van Luijk P, Pringle S, Deasy JO,et al. Sparing the region of the salivary gland containing stem cells preserves saliva production after radiotherapy for head and neck cancer. Sci Transl Med, 2015, 7(305): 305ra147.
10. Nanduri LS, Lombaert IM, van der Zwaag M,et al. Salisphere derived c-Kit⁺ cell transplantation restores tissue homeostasis in irradiated salivary gland. Radiother Oncol, 2013, 108(3): 458-463.
11. Xiao N, Lin Y, Cao H,et al. Neurotrophic factor GDNF promotes survival of salivary stem cells. J Clin Invest, 2014, 124(8): 3364-3377.
12. Coppes RP, Stokman MA. Stem cells and the repair of radiation-induced salivary gland damage. Oral Dis, 2011, 17(2): 143-153.
13. Nanduri LS, Maimets M, Pringle SA,et al. Regeneration of irradiated salivary glands with stem cell marker expressing cells. Radiother Oncol, 2011, 99(3): 367-372.
14. Lu L, Li Y, Du MJ,et al. Characterization of a Self-renewing and Multi-potent Cell Population Isolated from Human Minor Salivary Glands. Sci Rep, 2015, 5: 10106.
15. Banh A, Xiao N, Cao H,et al. A novel aldehyde dehydrogenase-3 activator leads to adult salivary stem cell enrichmentin vivo. Clin Cancer Res, 2011, 17(23): 7265-7272.
16. 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 Methods, 2012, 18(9): 710-718.
17. Lim JY, Yi T, Choi JS,et al. Intraglandular transplantation of bone marrow-derived clonal mesenchymal stem cells for amelioration of post-irradiation salivary gland damage. Oral Oncol, 2013, 49(2): 136-143.
18. Zhang NN, Huang GL, Han QB,et al. Functional regeneration of irradiated salivary glands with human amniotic epithelial cells transplantation. Int J Clin Exp Pathol, 2013, 6(10): 2039-2347.
19. Tran SD, Liu Y, Xia D,et al. Paracrine effects of bone marrow soup restore organ function, regeneration, and repair in salivary glands damaged by irradiation. PLoS One, 2013, 8(4): e61632.
20. Zheng C, Cotrim AP, Rowzee A,et al. Prevention of radiation-induced salivary hypofunction following hKGF gene delivery to murine submandibular glands. Clin Cancer Res, 2011, 17(9): 2842-2851.
21. Hai B, Yang Z, Shangguan L,et al. Concurrent transient activation of Wnt/beta-catenin pathway prevents radiation damage to salivary glands. Int J Radiat Oncol Biol Phys, 2012, 83(1): e109-116.
22. Garcia-Gallastegui P, Ibarretxe G, GarciaRamirez JJ,et al. DLK1 regulates branching morphogenesis and parasympathetic innervation of salivary glands through inhibition of NOTCH signalling. Biol Cell, 2014, 106(8): 237-253.
23. Hai B, Qin L, Yang Z,et al. Transient activation of hedgehog pathway rescued irradiation-induced hyposalivation by preserving salivary stem/progenitor cells and parasympathetic innervation. Clin Cancer Res, 2014, 20(1): 140-150.
24. Kojima T, Kanemaru S, Hirano S,et al. The protective efﬁcacy of basic ﬁbroblast growth factor in radiation-induced salivary gland dysfunction in mice. Laryngoscope, 2011, 121(9): 1870-1875.
25. Marmary Y, Adar R, Gaska S,et al. Radiation-induced loss of salivary gland function is driven by cellular senescence and prevented by IL6 modulation. Cancer Res, 2016, 76(5): 1170-1180.
26. Hill G, Headon D, Harris ZI,et al. Pharmacological activation of the EDA/EDAR signaling pathway restores salivary gland function following radiation-induced damage. PLoS One, 2014, 9(11): e112840.
27. Kawakami M, Ishikawa H, Tachibana T,et al. Functional transplantation of salivary gland cells differentiated from mouse early ES cellsin vitro. Hum Cell, 2013, 26(2): 80-90.
28. Beauchamp P, Mortitz W, Kelm JM,et al. Development and Characterization of a Scaffold-Free 3D Spheroid Model of Induced Pluripotent Stem Cell-Derived Human Cardiomyocytes. Tissue Eng Part C Methods, 2015, 21(8): 852-861.
29. Ono H, Obana A, Usami Y,et al. Regenerating salivary glands in the microenvironment of induced pluripotent stem cells. Biomed Res Int, 2015, 2015: 293570.
30. Eiraku M, Watanabe K, Matsuo-Takasaki M,et al. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell, 2008, 3(5): 519-532.
31. Lancaster MA, Knoblich JA. Organogenesis in a dish: modeling development and disease using organoid technologies. Science, 2014, 345(6194): 1247125.
32. 王军胜, 黄桂林, 张霓霓, 等. 三维培养条件下胚胎鼠唾液腺上皮细胞的自组装. 中国组织工程研究与临床康复, 2011, 15(40): 7549-7553.
33. Rookmaaker MB, Schutgens F, Verhaar MC,et al. Development and application of human adult stem or progenitor cell organoids. Nat Rev Nephrol, 2015, 11(9): 546-554.
34. Jang SI, Ong HL, Gallo A,et al. Establishment of functional acinar-like cultures from human salivary glands. J Dent Res, 2015, 94(2): 304-311.
35. Okumura K, Shinohara M, Endo F. Capability of tissue stem cells to organize into salivary rudiments. Stem Cells Int, 2012, 2012: 502136.
36. Sneddon JB, Borowiak M, Melton DA. Self-renewal of embryonic-stem-cell-derived progenitors by organ-matched mesenchyme. Nature, 2012, 491(7426): 765-768.
37. Skardal A, Smith L, Bharadwaj S,et al. Tissue specific synthetic ECM hydrogels for 3Din vitro maintenance of hepatocyte function. Biomaterials, 2012, 33(18): 4565-4575.
38. Cantara SI, Soscia DA, Sequeira SJ,et al. Selective functionalization of nanofiber scaffolds to regulate salivary gland epithelial cell proliferation and polarity. Biomaterials, 2012, 33(33): 8372-8382.
39. Pradhan S, Liu C, Zhang C,et al. Lumen formation in three-dimensional cultures of salivary acinar cells. Otolaryngol Head Neck Surg, 2010, 142(2): 191-195.
40. Yang TL, Hsiao YC. Chitosan facilitates structure formation of the salivary gland by regulating the basement membrane components. Biomaterials, 2015, 66: 29-40.
41. Maria OM, Maria O, Liu Y,et al. Matrigel improves functional properties of human submandibular salivary gland cell line. Int J Biochem Cell Biol, 2011, 43(4): 622-631.
42. Gao Z, Wu T, Xu J,et al. Generation of bioartiﬁcial salivary gland using whole-organ decellularized bioscaffold. Cells Tissues Organs, 2014, 200(3-4): 171-180.
43. Soscia DA, Sequeira SJ, Schramm RA,et al. Salivary gland cell differentiation and organization on micropatterned PLGA nanofiber craters. Biomaterials, 2013, 34(28): 6773-6784.
44. Peters SB, Naim N, Nelson DA,et al. Biocompatible tissue scaffold compliance promotes salivary gland morphogenesis and differentiation. Tissue Eng Part A, 2014, 20(11-12): 1632-1642.
45. Daley WP, Gervais EM, Centanni SW,et al. ROCK1-directed basement membrane positioning coordinates epithelial tissue polarity. Development, 2012, 139(2): 411-422.
46. Cosson S, Allazetta S, Lutolf M P,et al. Patterning of cell-instructive hydrogels by hydrodynamic flow focusing. Lab Chip, 2013, 13(11): 2099-2105.
47. Zheng Y, Chen J, Craven M,et al.In vitro microvessels for the study of angiogenesis and thrombosis. Proc Natl Acad Sci U S A, 2012, 109(24): 9342-9347.
48. Pringle S, Maimets M, van der Zwaag M,et al. Human salivary gland stem cells functionally restore radiation damaged salivary glands. Stem Cells, 2016, 34(3): 640-652.

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