Browse > Article
http://dx.doi.org/10.1186/2055-7124-18-9

Adult stem cells and tissue engineering strategies for salivary gland regeneration: a review  

Yoo, Chankee (Department of Biomedical Engineering, University of Alabama at Birmingham)
Vines, Jeremy B. (Department of Biomedical Engineering, University of Alabama at Birmingham)
Alexander, Grant (Department of Biomedical Engineering, University of Alabama at Birmingham)
Murdock, Kyle (Department of Biomedical Engineering, University of Alabama at Birmingham)
Hwang, Patrick (Department of Biomedical Engineering, University of Alabama at Birmingham)
Jun, Ho-Wook (Department of Biomedical Engineering, University of Alabama at Birmingham)
Publication Information
Biomaterials Research / v.18, no.3, 2014 , pp. 55-66 More about this Journal
Abstract
Saliva is an important compound produced by the salivary glands and performs numerous functions. Hyposalivation (dry mouth syndrome) is a deleterious condition often resulting from radiotherapy for patients with head and neck cancer, Sjogren's Syndrome, or as a side effect of certain medications. Hyposalivation negatively affects speaking, mastication, and swallowing in afflicted patients, greatly reducing their quality of life. Current treatments for this pathology include modifying lifestyle, synthetic saliva supplementation, and the utilization of salivary gland stimulants and sialagogues. However, many of these treatments do not address the underlying issues and others are pervaded by numerous side effects. In order to address the shortcomings related to current treatment modalities, many groups have diverted their attention to utilizing tissue engineering and regenerative medicine approaches. Tissue engineering is defined as the application of life sciences and materials engineering toward the development of tissue substitutes that are capable of mimicking the structure and function of their natural analogues within the body. The general underlying strategy behind the development of tissue engineered organ substitutes is the utilization of a combination of cells, biomaterials, and biochemical cues intended to recreate the natural organ environment. The purpose of this review is to highlight current bioengineering approaches for salivary gland tissue engineering and the adult stem cell sources used for this purpose. Additionally, future considerations in regard to salivary gland tissue engineering strategies are discussed.
Keywords
Hyposalivation; Mesenchymal stem cells; Tissue engineering; Salivary gland; Xerostomia;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Edgar W, O'Mullane D, Dawes C: Saliva and oral health. London: British Dental Association; 2004.
2 Thomson WM, Lawrence HP, Broadbent JM, Poulton R: The impact of xerostomia on oral-health-related quality of life among younger adults. Health Qual Life Outcomes 2006, 4:86.   DOI   ScienceOn
3 Berk L: Systemic pilocarpine for treatment of xerostomia. Expert Opin Drug Metab Toxicol 2008, 4:1333-1340.   DOI
4 Pillemer SR, Matteson EL, Jacobsson LT, Martens PB, Melton LJ 3rd, O'Fallon WM, Fox PC: Incidence of physician-diagnosed primary Sjogren syndrome in residents of Olmsted County, Minnesota. Mayo Clin Proc 2001, 76:593-599.   DOI
5 Clauss F, Maniere MC, Obry F, Waltmann E, Hadj-Rabia S, Bodemer C, Alembik Y, Lesot H, Schmittbuhl M: Dento-craniofacial phenotypes and underlying molecular mechanisms in hypohidrotic ectodermal dysplasia (HED): a review. J Dent Res 2008, 87:1089-1099.   DOI
6 Jensen SB, Pedersen AM, Vissink A, Andersen E, Brown CG, Davies AN, Dutilh J, Fulton JS, Jankovic L, Lopes NN, Mello AL, Muniz LV, Murdoch- Kinch CA, Nair RG, Napenas JJ, Nogueira-Rodrigues A, Saunders D, Stirling B, von Bultzingslowen I, Weikel DS, Elting LS, Spijkervet FK, Brennan MT, Salivary Gland Hypofunction/Xerostomia S, Oral Care Study G, Multinational Association of Supportive Care in Cancer/International Society of Oral O: A systematic review of salivary gland hypofunction and xerostomia induced by cancer therapies: management strategies and economic impact. Support Care Cancer 2010, 18:1061-1079.   DOI   ScienceOn
7 Pinheiro M, Freire-Maia N: Ectodermal dysplasias: a clinical classification and a causal review. Am J Med Genet 1994, 53:153-162.   DOI   ScienceOn
8 Nordgarden H, Storhaug K, Lyngstadaas SP, Jensen JL: Salivary gland function in persons with ectodermal dysplasias. Eur J Oral Sci 2003, 111:371-376.   DOI   ScienceOn
9 Vissink A, Mitchell JB, Baum BJ, Limesand KH, Jensen SB, Fox PC, Elting LS, Langendijk JA, Coppes RP, Reyland ME: Clinical management of salivary gland hypofunction and xerostomia in head-and-neck cancer patients: successes and barriers. Int J Radiat Oncol Biol Phys 2010, 78:983-991.   DOI
10 Silvestre FJ, Minguez MP, Sune-Negre JM: Clinical evaluation of a new artificial saliva in spray form for patients with dry mouth. Med Oral Patol Oral Cir Bucal 2009, 14:E8-E11.
11 Jansma J, Vissink A, Spijkervet FK, Roodenburg JL, Panders AK, Vermey A, Szabo BG, Gravenmade EJ: Protocol for the prevention and treatment of oral sequelae resulting from head and neck radiation therapy. Cancer 1992, 70:2171-2180.   DOI   ScienceOn
12 Jellema AP, Slotman BJ, Doornaert P, Leemans CR, Langendijk JA: Impact of radiation-induced 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.   DOI
13 Nelson J, Manzella K, Baker OJ: Current cell models for bioengineering a salivary gland: a mini-review of emerging technologies. Oral Dis 2013, 19:236-244.   DOI
14 Langer R, Vacanti JP: Tissue engineering. Science 1993, 260:920-926.   DOI   ScienceOn
15 Hirayama M, Oshima M, Tsuji T: Development and prospects of organ replacement regenerative therapy. Cornea 2013, 32(Suppl 1):S13-S21.   DOI
16 Sreebny LM, Vissink A: Dry mouth, the malevolent symptom: a clinical guide. Ames, Iowa: John Wiley & Sons; 2010.
17 Holsinger FC, Bui DT: Anatomy, function, and evaluation of the salivary glands. In Salivary Gland Disorders. Springer; 2007:1-16. [http://link.springer.com/chapter/10.1007%2F978-3-540-47072-4_1]
18 Coppes RP, Stokman MA: Stem cells and the repair of radiation-induced salivary gland damage. Oral Dis 2011, 17:143-153.   DOI
19 Pringle S, Van Os R, Coppes RP: Concise review: Adult salivary gland stem cells and a potential therapy for xerostomia. Stem Cells 2013, 31:613-619.   DOI
20 Coppes RP, Zeilstra LJ, Kampinga HH, Konings AW: Early to late sparing of radiation damage to the parotid gland by adrenergic and muscarinic receptor agonists. Br J Cancer 2001, 85:1055-1063.   DOI
21 Burlage FR, Coppes RP, Meertens H, Stokman MA, Vissink A: Parotid and submandibular/sublingual salivary flow during high dose radiotherapy. Radiother Oncol 2001, 61:271-274.   DOI   ScienceOn
22 Zeilstra LJ, Vissink A, Konings AW, Coppes RP: Radiation induced cell loss in rat submandibular gland and its relation to gland function. Int J Radiat Biol 2000, 76:419-429.   DOI
23 Stephens LC, Schultheiss TE, Price RE, Ang KK, Peters LJ: Radiation apoptosis of serous acinar cells of salivary and lacrimal glands. Cancer 1991, 67:1539-1543.   DOI   ScienceOn
24 Stephens LC, Schultheiss TE, Small SM, Ang KK, Peters LJ: Response of parotid gland organ culture to radiation. Radiat Res 1989, 120:140-153.   DOI
25 Konings AW, Coppes RP, Vissink A: On the mechanism of salivary gland radiosensitivity. Int J Radiat Oncol Biol Phys 2005, 62:1187-1194.   DOI
26 Konings AW, Faber H, Cotteleer F, Vissink A, Coppes RP: 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.   DOI
27 Rotter N, Oder J, Schlenke P, Lindner U, Bohrnsen F, Kramer J, Rohwedel J, Huss R, Brandau S, Wollenberg B, Lang S: Isolation and characterization of adult stem cells from human salivary glands. Stem Cells Dev 2008, 17:509-518.   DOI   ScienceOn
28 Lombaert IM, Brunsting JF, Wierenga PK, Faber H, Stokman MA, Kok T, Visser WH, Kampinga HH, de Haan G, Coppes RP: Rescue of salivary gland function after stem cell transplantation in irradiated glands. PLoS One 2008, 3:e2063.   DOI
29 Sumita Y, Liu Y, Khalili S, Maria OM, Xia D, Key S, Cotrim AP, Mezey E, Tran SD: Bone marrow-derived cells rescue salivary gland function in mice with head and neck irradiation. Int J Biochem Cell Biol 2011, 43:80-87.   DOI
30 Jeong J, Baek H, Kim YJ, Choi Y, Lee H, Lee E, Kim ES, Hah JH, Kwon TK, Choi IJ, Kwon H: Human salivary gland stem cells ameliorate hyposalivation of radiation-damaged rat salivary glands. Exp Mol Med 2013, 45:e58.   DOI
31 Kawakami M, Ishikawa H, Tachibana T, Tanaka A, Mataga I: Functional transplantation of salivary gland cells differentiated from mouse early ES cells in vitro. Hum Cell 2013, 26:80-90.   DOI
32 Xu J, Wang D, Liu D, Fan Z, Zhang H, Liu O, Ding G, Gao R, Zhang C, Ding Y, Bromberg JS, Chen W, Sun L, Wang S: Allogeneic mesenchymal stem cell treatment alleviates experimental and clinical Sjogren syndrome. Blood 2012, 120:3142-3151.   DOI
33 Lin CY, Chang FH, Chen CY, Huang CY, Hu FC, Huang WK, Ju SS, Chen MH: Cell therapy for salivary gland regeneration. J Dent Res 2011, 90:341-346.   DOI
34 Lim JY, Yi T, Choi JS, Jang YH, Lee S, Kim HJ, Song SU, Kim YM: Intraglandular transplantation of bone marrow-derived clonal mesenchymal stem cells for amelioration of post-irradiation salivary gland damage. Oral Oncol 2013, 49:136-143.   DOI
35 Khalili S, Liu Y, Kornete M, Roescher N, Kodama S, Peterson A, Piccirillo CA, Tran SD: Mesenchymal stromal cells improve salivary function and reduce lymphocytic infiltrates in mice with Sjogren's-like disease. PLoS One 2012, 7:e38615.   DOI
36 Kojima T, Kanemaru S, Hirano S, Tateya I, Ohno S, Nakamura T, Ito J: Regeneration of radiation damaged salivary glands with adipose-derived stromal cells. Laryngoscope 2011, 121:1864-1869.
37 Lim JY, Ra JC, Shin IS, Jang YH, An HY, Choi JS, Kim WC, Kim YM: Systemic transplantation of human adipose tissue-derived mesenchymal stem cells for the regeneration of irradiation-induced salivary gland damage. PLoS One 2013, 8:e71167.   DOI
38 Romanov YA, Svintsitskaya VA, Smirnov VN: Searching for alternative sources of postnatal human mesenchymal stem cells: candidate MSC-like cells from umbilical cord. Stem Cells 2003, 21:105-110.   DOI   ScienceOn
39 Kogler G, Sensken S, Airey JA, Trapp T, Muschen M, Feldhahn N, Liedtke S, Sorg RV, Fischer J, Rosenbaum C, Greschat S, Knipper A, Bender J, Degistirici O, Gao J, Caplan AI, Colletti EJ, Almeida-Porada G, Muller HW, Zanjani E, Wernet P: A new human somatic stem cell from placental cord blood with intrinsic pluripotent differentiation potential. J Exp Med 2004, 200:123-135.   DOI   ScienceOn
40 Tsai MS, Lee JL, Chang YJ, Hwang SM: Isolation of human multipotent mesenchymal stem cells from second-trimester amniotic fluid using a novel two-stage culture protocol. Hum Reprod 2004, 19:1450-1456.   DOI   ScienceOn
41 In't Anker PS, Scherjon SA, Kleijburg-van der Keur C, de Groot-Swings GM, Claas FH, Fibbe WE, Kanhai HH: Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 2004, 22:1338-1345.   DOI
42 Fukuchi Y, Nakajima H, Sugiyama D, Hirose I, Kitamura T, Tsuji K: Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 2004, 22:649-658.   DOI   ScienceOn
43 Takahashi K, Igura K, Zhang X, Mitsuru A, Takahashi TA: Effects of osteogenic induction on mesenchymal cells from fetal and maternal parts of human placenta. Cell Transplant 2004, 13:337-341.   DOI
44 Huang GL, Zhang NN, Wang JS, Yao L, Zhao YJ, Wang YY: Transdifferentiation of human amniotic epithelial cells into acinar cells using a double-chamber system. Cell Reprogram 2012, 14:377-383.
45 Zhang NN, Huang GL, Han QB, Hu X, Yi J, Yao L, He Y: Functional regeneration of irradiated salivary glands with human amniotic epithelial cells transplantation. Int J Clin Exp Pathol 2013, 6:2039-2047.
46 Murphy SV, Atala A: Amniotic fluid and placental membranes: unexpected sources of highly multipotent cells. Semin Reprod Med 2013, 31:62-68.   DOI
47 Murphy S, Rosli S, Acharya R, Mathias L, Lim R, Wallace E, Jenkin G: Amnion epithelial cell isolation and characterization for clinical use. Curr Protoc Stem Cell Biol 2010, Chapter 1:Unit 1E 6.
48 Ilancheran S, Michalska A, Peh G, Wallace EM, Pera M, Manuelpillai U: Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol Reprod 2007, 77:577-588.   DOI   ScienceOn
49 Dawson LJ, Smith PM, Moots RJ, Field EA: Sjogren's syndrome-time for a new approach. Rheumatology (Oxford) 2000, 39:234-237.   DOI
50 Fox RI, Konttinen Y, Fisher A: Use of muscarinic agonists in the treatment of Sjogren's syndrome. Clin Immunol 2001, 101:249-263.   DOI
51 Braga MA, Tarzia O, Bergamaschi CC, Santos FA, Andrade ED, Groppo FC: Comparison of the effects of pilocarpine and cevimeline on salivary flow. Int J Dent Hyg 2009, 7:126-130.   DOI
52 Ship JA: Diagnosing, managing, and preventing salivary gland disorders. Oral Dis 2002, 8:77-89.   DOI   ScienceOn
53 Richards Grayson AC, Choi IS, Tyler BM, Wang PP, Brem H, Cima MJ, Langer R: Multi-pulse drug delivery from a resorbable polymeric microchip device. Nat Mater 2003, 2:767-772.   DOI
54 Gibson J, Halliday JA, Ewert K, Robertson S: A controlled release pilocarpine buccal insert in the treatment of Sjogren's syndrome. Br Dent J 2007, 202:E17. discussion 404-405.   DOI
55 Tabata Y: Tissue regeneration based on growth factor release. Tissue Eng 2003, 9(Suppl 1):S5-S15.   DOI   ScienceOn
56 West JL: Drug delivery: pulsed polymers. Nat Mater 2003, 2:709-710.   DOI
57 Hirsch LR, Gobin AM, Lowery AR, Tam F, Drezek RA, Halas NJ, West JL: Metal nanoshells. Ann Biomed Eng 2006, 34:15-22.   DOI   ScienceOn
58 Sershen SR, Mensing GA, Ng M, Halas NJ, Beebe DJ, West JL: Independent Optical Control of Microfluidic Valves Formed from Optomechanically Responsive Nanocomposite Hydrogels. Adv Mater 2005, 17:1366-1368.   DOI   ScienceOn
59 Cantin M, Miranda P, Suazo Galdames I, Zavando D, Arenas P, Velasquez L, Vilos C: In vivo biocompatibility of the PLGA microparticles in parotid gland. Int J Clin Exp Pathol 2013, 6:2412-2418.
60 Samuni Y, Baum BJ: Gene delivery in salivary glands: from the bench to the clinic. Biochim Biophys Acta 1812, 2011:1515-1521.   DOI
61 Woods NB, Bottero V, Schmidt M, von Kalle C, Verma IM: Gene therapy: therapeutic gene causing lymphoma. Nature 2006, 440:1123.   DOI
62 Thomas CE, Ehrhardt A, Kay MA: Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 2003, 4:346-358.   DOI   ScienceOn
63 Somia N, Verma IM: Gene therapy: trials and tribulations. Nat Rev Genet 2000, 1:91-99.
64 Kagami H, Atkinson JC, Michalek SM, Handelman B, Yu S, Baum BJ, O'Connell B: Repetitive adenovirus administration to the parotid gland: role of immunological barriers and induction of oral tolerance. Hum Gene Ther 1998, 9:305-313.   DOI
65 Voutetakis A, Zheng C, Mineshiba F, Cotrim AP, Goldsmith CM, Schmidt M, Afione S, Roescher N, Metzger M, Eckhaus MA, Chiorini JA, Dunbar CE, Donahue RE, Baum BJ: Adeno-associated virus serotype 2-mediated gene transfer to the parotid glands of nonhuman primates. Hum Gene Ther 2007, 18:142-150.   DOI
66 Cotrim AP, Sowers A, Mitchell JB, Baum BJ: Prevention of irradiationinduced salivary hypofunction by microvessel protection in mouse salivary glands. Mol Ther 2007, 15:2101-2106.   DOI
67 Delporte C, O'Connell BC, He X, Lancaster HE, O'Connell AC, Agre P, Baum BJ: Increased fluid secretion after adenoviral-mediated transfer of the aquaporin-1 cDNA to irradiated rat salivary glands. Proc Natl Acad Sci U S A 1997, 94:3268-3273.   DOI
68 Shan Z, Li J, Zheng C, Liu X, Fan Z, Zhang C, Goldsmith CM, Wellner RB, Baum BJ, Wang S: Increased fluid secretion after adenoviral-mediated transfer of the human aquaporin-1 cDNA to irradiated miniature pig parotid glands. Mol Ther 2005, 11:444-451.   DOI
69 Epperly MW, Carpenter M, Agarwal A, Mitra P, Nie S, Greenberger JS: Intraoral manganese superoxide dismutase-plasmid/liposome (MnSOD-PL) radioprotective gene therapy decreases ionizing irradiation-induced murine mucosal cell cycling and apoptosis. In Vivo 2004, 18:401-410.
70 Nguyen CQ, Yin H, Lee BH, Chiorini JA, Peck AB: IL17: potential therapeutic target in Sjogren's syndrome using adenovirus-mediated gene transfer. Lab Invest 2011, 91:54-62.   DOI   ScienceOn
71 Kok MR, Yamano S, Lodde BM, Wang J, Couwenhoven RI, Yakar S, Voutetakis A, Leroith D, Schmidt M, Afione S, Pillemer SR, Tsutsui MT, Tak PP, Chiorini JA, Baum BJ: Local adeno-associated virus-mediated interleukin 10 gene transfer has disease-modifying effects in a murine model of Sjogren's syndrome. Hum Gene Ther 2003, 14:1605-1618.   DOI
72 Lodde BM, Mineshiba F, Wang J, Cotrim AP, Afione S, Tak PP, Baum BJ: Effect of human vasoactive intestinal peptide gene transfer in a murine model of Sjogren's syndrome. Ann Rheum Dis 2006, 65:195-200.   DOI
73 Baum BJ, Zheng C, Alevizos I, Cotrim AP, Liu S, McCullagh L, Goldsmith CM, McDermott N, Chiorini JA, Nikolov NP, Illei GG: Development of a gene transfer-based treatment for radiation-induced salivary hypofunction. Oral Oncol 2010, 46:4-8.   DOI
74 Zheng C, Nikolov NP, Alevizos I, Cotrim AP, Liu S, McCullagh L, Chiorini JA, Illei GG, Baum BJ: Transient detection of E1-containing adenovirus in saliva after the delivery of a first-generation adenoviral vector to human parotid gland. J Gene Med 2010, 12:3-10.   DOI
75 Lombaert IM, Wierenga PK, Kok T, Kampinga HH, deHaan G, Coppes RP: 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.   DOI
76 Ankrum JA, Ong JF, Karp JM: Mesenchymal stem cells: immune evasive, not immune privileged. Nat Biotechnol 2014, 32:252-260   DOI   ScienceOn
77 Lombaert IM, Brunsting JF, Wierenga PK, Kampinga HH, de Haan G, Coppes RP: Cytokine treatment improves parenchymal and vascular damage of salivary glands after irradiation. Clin Cancer Res 2008, 14:7741-7750.   DOI
78 Nakao K, Morita R, Saji Y, Ishida K, Tomita Y, Ogawa M, Saitoh M, Tomooka Y, Tsuji T: The development of a bioengineered organ germ method. Nat Methods 2007, 4:227-230.   DOI   ScienceOn
79 Ogawa M, Oshima M, Imamura A, Sekine Y, Ishida K, Yamashita K, Nakajima K, Hirayama M, Tachikawa T, Tsuji T: Functional salivary gland regeneration by transplantation of a bioengineered organ germ. Nat Commun 2013, 4:2498.
80 Keating A: Mesenchymal stromal cells: new directions. Cell Stem Cell 2012, 10:709-716.   DOI
81 Caplan AI, Correa D: The MSC: an injury drugstore. Cell Stem Cell 2011, 9:11-15.   DOI   ScienceOn
82 Phinney DG, Galipeau J, Krampera M, Martin I, Shi Y, Sensebe L: MSCs: science and trials. Nat Med 2013, 19:812.   DOI
83 Schu S, Nosov M, O'Flynn L, Shaw G, Treacy O, Barry F, Murphy M, O'Brien T, Ritter T: Immunogenicity of allogeneic mesenchymal stem cells. J Cell Mol Med 2012, 16:2094-2103.   DOI
84 Griffin MD, Ryan AE, Alagesan S, Lohan P, Treacy O, Ritter T: Anti-donor immune responses elicited by allogeneic mesenchymal stem cells: what have we learned so far? Immunol Cell Biol 2013, 91:40-51.   DOI
85 Zhang X, He H, Yen C, Ho W, Lee LJ: A biodegradable, immunoprotective, dual nanoporous capsule for cell-based therapies. Biomaterials 2008, 29:4253-4259.   DOI   ScienceOn
86 Calafiore R, Basta G: Artificial pancreas to treat type 1 diabetes mellitus. Methods Mol Med 2007, 140:197-236.   DOI
87 Nafea EH, Marson A, Poole-Warren LA, Martens PJ: Immunoisolating semi-permeable membranes for cell encapsulation: focus on hydrogels. J Control Release 2011, 154:110-122.   DOI
88 Levy O, Zhao W, Mortensen LJ, Leblanc S, Tsang K, Fu M, Phillips JA, Sagar V, Anandakumaran P, Ngai J, Cui CH, Eimon P, Angel M, Lin CP, Yanik MF, Karp JM: mRNA-engineered mesenchymal stem cells for targeted delivery of interleukin-10 to sites of inflammation. Blood 2013, 122:e23-e32.   DOI
89 Tanabe K, Takahashi K, Yamanaka S: Induction of pluripotency by defined factors. Proc Jpn Acad Ser B Phys Biol Sci 2014, 90:83-96.   DOI
90 Okano H, Nakamura M, Yoshida K, Okada Y, Tsuji O, Nori S, Ikeda E, Yamanaka S, Miura K: Steps toward safe cell therapy using induced pluripotent stem cells. Circ Res 2013, 112:523-533.   DOI
91 Janebodin K, Buranaphatthana W, Ieronimakis N, Hays AL, Reyes M: An in vitro culture system for long-term expansion of epithelial and mesenchymal salivary gland cells: role of TGF-beta1 in salivary gland epithelial and mesenchymal differentiation. Biomed Res Int 2013, 2013:815895.