Laminins are complex extracellular macromolecules that are major players in the control of a variety of core cell processes, including regulating rates of cell proliferation, differentiation, adhesion, and migration. Laminins, and related extracellular matrix components, have essential roles in tissue homeostasis; however, during wound healing, the same proteins are critical players in re-epithelialization and angiogenesis. Understanding how these proteins influence cell behavior in these different conditions holds great potential in identifying new strategies to enhance normal wound closure or to treat chronic/nonhealing wounds.
Recent Advances:
Laminin-derived bioactive peptides and, more recently, laminin-peptide conjugated scaffolds, have been designed to improve tissue regeneration after injuries. These peptides have been shown to be effective in decreasing inflammation and granulation tissue, and in promoting re-epithelialization, angiogenesis, and cell migration.
Critical Issues:
Although there is now a wealth of knowledge concerning laminin form and function, there are still areas of some controversy. These include the relative contribution of two laminin-based adhesive devices (focal contacts and hemidesmosomes) to the re-epithelialization process, the impact and implications of laminin proteolytic processing, and the importance of laminin polymer formation on cell behavior. In addition, the roles in wound healing of the laminin-related proteins, netrins, and LaNts are still to be fully defined.
Future Directions:
The future of laminin-based therapeutics potentially lies in the bioengineering of specific substrates to support laminin deposition for ex vivo expansion of autologous cells for graft formation and transplantation. Significant recent advances suggest that this goal is within sight.
KivirikkoS, McGrathJA, PulkkinenL, UittoJ, ChristianoAM. Mutational hotspots in the LAMB3 gene in the lethal (Herlitz) type of junctional epidermolysis bullosa. Hum Mol Genet, 1996; 5:231–237.
3.
MuhleC, JiangQJ, CharlesworthA, Bruckner-TudermanL, MeneguzziG, SchneiderH. Novel and recurrent mutations in the laminin-5 genes causing lethal junctional epidermolysis bullosa: molecular basis and clinical course of Herlitz disease. Hum Genet, 2005; 116:33–42.
4.
PulkkinenL, ChristianoAM, AirenneT, HaakanaH, TryggvasonK, UittoJ. Mutations in the gamma 2 chain gene (LAMC2) of kalinin/laminin 5 in the junctional forms of epidermolysis bullosa. Nat Genet, 1994; 6:293–297.
5.
KoMS, MarinkovichMP. Role of dermal-epidermal basement membrane zone in skin, cancer, and developmental disorders. Dermatol Clin, 2010; 28:1–16.
6.
TimplR, BrownJC. Supramolecular assembly of basement membranes. Bioessays, 1996; 18:123–132.
McLeanWH, IrvineAD, HamillKJ, et al.An unusual N-terminal deletion of the laminin alpha3a isoform leads to the chronic granulation tissue disorder laryngo-onycho-cutaneous syndrome. Hum Mol Genet, 2003; 12:2395–2409.
9.
RyanMC, LeeK, MiyashitaY, CarterWG. Targeted disruption of the LAMA3 gene in mice reveals abnormalities in survival and late stage differentiation of epithelial cells. J Cell Biol, 1999; 145:1309–1323.
10.
LaplanteAF, GermainL, AugerFA, MoulinV. Mechanisms of wound reepithelialization: hints from a tissue-engineered reconstructed skin to long-standing questions. FASEB J, 2001; 15:2377–2389.
11.
KurpakusMA, StockEL, JonesJC. Analysis of wound healing in an in vitro model: early appearance of laminin and a 125×10(3) Mr polypeptide during adhesion complex formation. J Cell Sci, 1990; 96(Pt 4):651–660.
12.
KainulainenT, HakkinenL, HamidiS, et al.Laminin-5 expression is independent of the injury and the microenvironment during reepithelialization of wounds. J Histochem Cytochem, 1998; 46:353–360.
13.
TaniguchiY, IdoH, SanzenN, et al.The C-terminal region of laminin beta chains modulates the integrin binding affinities of laminins. J Biol Chem, 2009; 284:7820–7831.
14.
KikkawaY, SanzenN, FujiwaraH, SonnenbergA, SekiguchiK. Integrin binding specificity of laminin-10/11: laminin-10/11 are recognized by alpha 3 beta 1, alpha 6 beta 1 and alpha 6 beta 4 integrins. J Cell Sci, 2000; 113(Pt 5):869–876.
15.
KariyaY, YasudaC, NakashimaY, IshidaK, TsubotaY, MiyazakiK. Characterization of laminin 5B and NH2-terminal proteolytic fragment of its alpha3B chain: promotion of cellular adhesion, migration, and proliferation. J Biol Chem, 2004; 279:24774–24784.
16.
SchenkS, HintermannE, BilbanM, et al.Binding to EGF receptor of a laminin-5 EGF-like fragment liberated during MMP-dependent mammary gland involution. J Cell Biol, 2003; 161:197–209.
17.
Gagnoux-PalaciosL, AllegraM, SpiritoF, et al.The short arm of the laminin gamma2 chain plays a pivotal role in the incorporation of laminin 5 into the extracellular matrix and in cell adhesion. J Cell Biol, 2001; 153:835–850.
18.
RyanMC, TizardR, VanDevanterDR, CarterWG. Cloning of the LamA3 gene encoding the alpha 3 chain of the adhesive ligand epiligrin. Expression in wound repair. J Biol Chem, 1994; 269:22779–22787.
19.
MacdonaldPR, LustigA, SteinmetzMO, KammererRA. Laminin chain assembly is regulated by specific coiled-coil interactions. J Struct Biol, 2010; 170:398–405.
20.
FaheyB, DegnanBM. Origin and evolution of laminin gene family diversity. Mol Biol Evol, 2012; 29:1823–1836.
21.
DomogatskayaA, RodinS, TryggvasonK. Functional diversity of laminins. Annu Rev Cell Dev Biol, 2012; 28:523–553.
22.
HamillKJ, KligysK, HopkinsonSB, JonesJC. Laminin deposition in the extracellular matrix: a complex picture emerges. J Cell Sci, 2009; 122:4409–4417.
23.
KallunkiP, SainioK, EddyR, et al.A truncated laminin chain homologous to the B2 chain: structure, spatial expression, and chromosomal assignment. J Cell Biol, 1992; 119:679–693.
24.
YurchencoPD, TsilibaryEC, CharonisAS, FurthmayrH. Laminin polymerization in vitro. Evidence for a two-step assembly with domain specificity. J Biol Chem, 1985; 260:7636–7644.
25.
SchittnyJC, YurchencoPD. Terminal short arm domains of basement membrane laminin are critical for its self-assembly. J Cell Biol, 1990; 110:825–832.
26.
YurchencoPD, ChengYS. Self-assembly and calcium-binding sites in laminin. A three-arm interaction model. J Biol Chem, 1993; 268:17286–17299.
27.
MinerJH, LiC, MuddJL, GoG, SutherlandAE. Compositional and structural requirements for laminin and basement membranes during mouse embryo implantation and gastrulation. Development, 2004; 131:2247–2256.
28.
MinerJH, PattonBL, LentzSI, et al.The laminin alpha chains: expression, developmental transitions, and chromosomal locations of alpha1-5, identification of heterotrimeric laminins 8–11, and cloning of a novel alpha3 isoform. J Cell Biol, 1997; 137:685–701.
29.
HallmannR, HornN, SelgM, WendlerO, PauschF, SorokinLM. Expression and function of laminins in the embryonic and mature vasculature. Physiol Rev, 2005; 85:979–1000.
30.
KariyaY, MoriT, YasudaC, et al.Localization of laminin alpha3B chain in vascular and epithelial basement membranes of normal human tissues and its down-regulation in skin cancers. J Mol Histol, 2008; 39:435–446.
31.
PouliotN, SaundersNA, KaurP. Laminin 10/11: an alternative adhesive ligand for epidermal keratinocytes with a functional role in promoting proliferation and migration. Exp Dermatol, 2002; 11:387–397.
32.
NguyenBP, GilSG, CarterWG. Deposition of laminin 5 by keratinocytes regulates integrin adhesion and signaling. J Biol Chem, 2000; 275:31896–31907.
33.
JonesJC, YokooKM, GoldmanRD. Is the hemidesmosome a half desmosome? An immunological comparison of mammalian desmosomes and hemidesmosomes. Cell Motil Cytoskeleton, 1986; 6:560–569.
34.
WilhelmsenK, LitjensSH, KuikmanI, MargadantC, van RheenenJ, SonnenbergA. Serine phosphorylation of the integrin beta4 subunit is necessary for epidermal growth factor receptor induced hemidesmosome disruption. Mol Biol Cell, 2007; 18:3512–3522.
35.
MargadantC, FrijnsE, WilhelmsenK, SonnenbergA. Regulation of hemidesmosome disassembly by growth factor receptors. Curr Opin Cell Biol, 2008; 20:589–596.
36.
TsurutaD, HashimotoT, HamillKJ, JonesJC. Hemidesmosomes and focal contact proteins: functions and cross-talk in keratinocytes, bullous diseases and wound healing. J Dermatol Sci, 2011; 62:1–7.
37.
RiddelleKS, HopkinsonSB, JonesJC. Hemidesmosomes in the epithelial cell line 804G: their fate during wound closure, mitosis and drug induced reorganization of the cytoskeleton. J Cell Sci, 1992; 103(Pt 2):475–490.
38.
HamillKJ, HopkinsonSB, DeBiaseP, JonesJC. BPAG1e maintains keratinocyte polarity through beta4 integrin-mediated modulation of Rac1 and cofilin activities. Mol Biol Cell, 2009; 20:2954–2962.
39.
HamillKJ, HopkinsonSB, JonkmanMF, JonesJC. Type XVII collagen regulates lamellipod stability, cell motility, and signaling to Rac1 by targeting bullous pemphigoid antigen 1e to alpha6beta4 integrin. J Biol Chem, 2011; 286:26768–26780.
40.
SehgalBU, DeBiasePJ, MatznoS, et al.Integrin beta4 regulates migratory behavior of keratinocytes by determining laminin-332 organization. J Biol Chem, 2006; 281:35487–35498.
41.
PullarCE, BaierBS, KariyaY, et al.beta4 integrin and epidermal growth factor coordinately regulate electric field-mediated directional migration via Rac1. Mol Biol Cell, 2006; 17:4925–4935.
42.
BeningoKA, DemboM, KaverinaI, SmallJV, WangYL. Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J Cell Biol, 2001; 153:881–888.
43.
DiPersioCM, ShahS, HynesRO. alpha 3A beta 1 integrin localizes to focal contacts in response to diverse extracellular matrix proteins. J Cell Sci, 1995; 108(Pt 6):2321–2336.
44.
ChomaDP, PumigliaK, DiPersioCM. Integrin alpha3beta1 directs the stabilization of a polarized lamellipodium in epithelial cells through activation of Rac1. J Cell Sci, 2004; 117:3947–3959.
45.
KligysKR, WuY, HopkinsonSB, KaurS, PlataniasLC, JonesJC. alpha6beta4 integrin, a master regulator of expression of integrins in human keratinocytes. J Biol Chem, 2012; 287:17975–17984.
GoldfingerLE, HopkinsonSB, deHartGW, CollawnS, CouchmanJR, JonesJC. The alpha3 laminin subunit, alpha6beta4 and alpha3beta1 integrin coordinately regulate wound healing in cultured epithelial cells and in the skin. J Cell Sci, 1999; 112(Pt 16):2615–2629.
48.
MargadantC, RaymondK, KreftM, SachsN, JanssenH, SonnenbergA. Integrin alpha3beta1 inhibits directional migration and wound re-epithelialization in the skin. J Cell Sci, 2009; 122:278–288.
49.
SteppMA, GibsonHE, GalaPH, et al.Defects in keratinocyte activation during wound healing in the syndecan-1-deficient mouse. J Cell Sci, 2002; 115:4517–4531.
BassMD, RoachKA, MorganMR, et al.Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J Cell Biol, 2007; 177:527–538.
52.
ZimmermannP, DavidG. The syndecans, tuners of transmembrane signaling. FASEB J, 1999; 13Suppl:S91–S100.
53.
SigleRO, GilSG, BhattacharyaM, et al.Globular domains 4/5 of the laminin alpha3 chain mediate deposition of precursor laminin 5. J Cell Sci, 2004; 117:4481–4494.
54.
UsuiML, MansbridgeJN, CarterWG, FujitaM, OlerudJE. Keratinocyte migration, proliferation, and differentiation in chronic ulcers from patients with diabetes and normal wounds. J Histochem Cytochem, 2008; 56:687–696.
55.
SenyurekI, KempfWE, KleinG, et al.Processing of laminin alpha chains generates peptides involved in wound healing and host defense. J Innate Immun, 2014 [Epub ahead of print]. (DOI:10.1159/000357032)
56.
OgawaT, TsubotaY, HashimotoJ, KariyaY, MiyazakiK. The short arm of laminin gamma2 chain of laminin-5 (laminin-332) binds syndecan-1 and regulates cellular adhesion and migration by suppressing phosphorylation of integrin beta4 chain. Mol Biol Cell, 2007; 18:1621–1633.
JiangQJ, IzakovicJ, ZenkerM, et al.Treatment of two patients with Herlitz junctional epidermolysis bullosa with artificial skin bioequivalents. J Pediatr, 2002; 141:553–559.
59.
FigueiraEC, CrottyA, ChallinorCJ, CoroneoMT, MurrellDF. Granulation tissue in the eyelid margin and conjunctiva in junctional epidermolysis bullosa with features of laryngo-onycho-cutaneous syndrome. Clin Exp Ophthalmol, 2007; 35:163–166.
60.
BarzegarM, MozafariN, KariminejadA, AsadikaniZ, OzoemenaL, McGrathJA. A new homozygous nonsense mutation in LAMA3A underlying laryngo-onycho-cutaneous syndrome. Br J Dermatol, 2013; 169:1353–1356.
HussainSA, CarafoliF, HohenesterE. Determinants of laminin polymerization revealed by the structure of the alpha5 chain amino-terminal region. EMBO Rep, 2011; 12:276–282.
64.
PouliotN, KusumaN. Laminin-511: a multi-functional adhesion protein regulating cell migration, tumor invasion and metastasis. Cell Adh Migr, 2013; 7:142–149.
65.
PouliotN, NiceEC, BurgessAW. Laminin-10 mediates basal and EGF-stimulated motility of human colon carcinoma cells via alpha(3)beta(1) and alpha(6)beta(4) integrins. Exp Cell Res, 2001; 266:1–10.
66.
SorokinLM, PauschF, FrieserM, KrogerS, OhageE, DeutzmannR. Developmental regulation of the laminin alpha5 chain suggests a role in epithelial and endothelial cell maturation. Dev Biol, 1997; 189:285–300.
67.
MinerJH, CunninghamJ, SanesJR. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J Cell Biol, 1998; 143:1713–1723.
68.
SatoN, NakamuraM, ChikamaT, NishidaT. Abnormal deposition of laminin and type IV collagen at corneal epithelial basement membrane during wound healing in diabetic rats. Jpn J Ophthalmol, 1999; 43:343–347.
69.
LjubimovAV, HuangZS, HuangGH, et al.Human corneal epithelial basement membrane and integrin alterations in diabetes and diabetic retinopathy. J Histochem Cytochem, 1998; 46:1033–1041.
70.
Paquet-FifieldS, SchluterH, LiA, et al.A role for pericytes as microenvironmental regulators of human skin tissue regeneration. J Clin Invest, 2009; 119:2795–2806.
71.
LiA, PouliotN, RedversR, KaurP. Extensive tissue-regenerative capacity of neonatal human keratinocyte stem cells and their progeny. J Clin Invest, 2004; 113:390–400.
72.
DoiM, ThybollJ, KortesmaaJ, et al.Recombinant human laminin-10 (alpha5beta1gamma1). Production, purification, and migration-promoting activity on vascular endothelial cells. J Biol Chem, 2002; 277:12741–12748.
73.
GrecianoPG, MoyanoJV, BuschmannMM, et al.Laminin 511 partners with laminin 332 to mediate directional migration of Madin-Darby canine kidney epithelial cells. Mol Biol Cell, 2012; 23:121–136.
74.
KortesmaaJ, YurchencoP, TryggvasonK. Recombinant laminin-8 (alpha(4)beta(1)gamma(1)). Production, purification, and interactions with integrins. J Biol Chem, 2000; 275:14853–14859.
75.
WondimuZ, GeberhiwotT, IngerpuuS, et al.An endothelial laminin isoform, laminin 8 (alpha4beta1gamma1), is secreted by blood neutrophils, promotes neutrophil migration and extravasation, and protects neutrophils from apoptosis. Blood, 2004; 104:1859–1866.
76.
ThybollJ, KortesmaaJ, CaoR, et al.Deletion of the laminin alpha4 chain leads to impaired microvessel maturation. Mol Cell Biol, 2002; 22:1194–1202.
77.
JakobssonL, DomogatskayaA, TryggvasonK, EdgarD, Claesson-WelshL. Laminin deposition is dispensable for vasculogenesis but regulates blood vessel diameter independent of flow. FASEB J, 2008; 22:1530–1539.
78.
AumailleyM, NurcombeV, EdgarD, PaulssonM, TimplR. The cellular interactions of laminin fragments. Cell adhesion correlates with two fragment-specific high affinity binding sites. J Biol Chem, 1987; 262:11532–11538.
79.
PaulssonM, AumailleyM, DeutzmannR, TimplR, BeckK, EngelJ. Laminin-nidogen complex. Extraction with chelating agents and structural characterization. Eur J Biochem, 1987; 166:11–19.
80.
KittelbergerR, DavisPF, StehbensWE. Distribution of type IV collagen, laminin, nidogen and fibronectin in the haemodynamically stressed vascular wall. Histol Histopathol, 1990; 5:161–167.
81.
TaltsJF, SasakiT, MiosgeN, et al.Structural and functional analysis of the recombinant G domain of the laminin alpha4 chain and its proteolytic processing in tissues. J Biol Chem, 2000; 275:35192–35199.
82.
SenyurekI, KleinG, KalbacherH, DeegM, SchittekB. Peptides derived from the human laminin alpha4 and alpha5 chains exhibit antimicrobial activity. Peptides, 2010; 31:1468–1472.
GonzalesM, WekslerB, TsurutaD, et al.Structure and function of a vimentin-associated matrix adhesion in endothelial cells. Mol Biol Cell, 2001; 12:85–100.
85.
GonzalezAM, GonzalesM, HerronGS, et al.Complex interactions between the laminin alpha 4 subunit and integrins regulate endothelial cell behavior in vitro and angiogenesis in vivo. Proc Natl Acad Sci U S A, 2002; 99:16075–16080.
86.
LiJ, ZhouL, TranHT, et al.Overexpression of laminin-8 in human dermal microvascular endothelial cells promotes angiogenesis-related functions. J Invest Dermatol, 2006; 126:432–440.
87.
LianJ, DaiX, LiX, HeF. Identification of an active site on the laminin alpha4 chain globular domain that binds to alphavbeta3 integrin and promotes angiogenesis. Biochem Biophys Res Commun, 2006; 347:248–253.
88.
CastetsM, MehlenP. Netrin-1 role in angiogenesis: to be or not to be a pro-angiogenic factor?. Cell Cycle, 2010; 9:1466–1471.
89.
RajasekharanS, KennedyTE. The netrin protein family. Genome Biol, 2009; 10:239.
90.
CastetsM, BroutierL, MolinY, et al.DCC constrains tumour progression via its dependence receptor activity. Nature, 2012; 482:534–537.
91.
KelkerW, Van DykeDL, WorshamMJ, et al.Loss of 18q and homozygosity for the DCC locus: possible markers for clinically aggressive squamous cell carcinoma. Anticancer Res, 1996; 16:2365–2372.
92.
ParkHL, KimMS, YamashitaK, et al.DCC promoter hypermethylation in esophageal squamous cell carcinoma. Int J Cancer, 2008; 122:2498–2502.
93.
LiYN, Pinzon-DuarteG, DattiloM, ClaudepierreT, KochM, BrunkenWJ. The expression and function of netrin-4 in murine ocular tissues. Exp Eye Res, 2012; 96:24–35.
94.
HanY, ShaoY, LinZ, et al.Netrin-1 simultaneously suppresses corneal inflammation and neovascularization. Invest Ophthalmol Vis Sci, 2012; 53:1285–1295.
95.
ShekarabiM, KennedyTE. The netrin-1 receptor DCC promotes filopodia formation and cell spreading by activating Cdc42 and Rac1. Mol Cell Neurosci, 2002; 19:1–17.
96.
PicardM, PetrieRJ, Antoine-BertrandJ, Saint-Cyr-ProulxE, VillemureJF, Lamarche-VaneN. Spatial and temporal activation of the small GTPases RhoA and Rac1 by the netrin-1 receptor UNC5a during neurite outgrowth. Cell Signal, 2009; 21:1961–1973.
97.
HuY, YlivinkkaI, ChenP, et al.Netrin-4 promotes glioblastoma cell proliferation through integrin beta4 signaling. Neoplasia, 2012; 14:219–227.
98.
StaquiciniFI, Dias-NetoE, LiJ, et al.Discovery of a functional protein complex of netrin-4, laminin gamma1 chain, and integrin alpha6beta1 in mouse neural stem cells. Proc Natl Acad Sci U S A, 2009; 106:2903–2908.
99.
SchneidersFI, MaertensB, BoseK, et al.Binding of netrin-4 to laminin short arms regulates basement membrane assembly. J Biol Chem, 2007; 282:23750–23758.
100.
HagedornEJ, ZielJW, MorrisseyMA, et al.The netrin receptor DCC focuses invadopodia-driven basement membrane transmigration in vivo. J Cell Biol, 2013; 201(6):903–913.
101.
HamillKJ, LangbeinL, JonesJC, McLeanWH. Identification of a novel family of laminin N-terminal alternate splice isoforms: structural and functional characterization. J Biol Chem, 2009; 284:35588–35596.
102.
BlinovaMI, ParamonovBA, KukharevaLV, Gorelik IuV, Nikitina IuM, VoronkinaIV. [Effect of fibroblasts, collagen, and laminin on the healing of wounds formed after dissection of split skin flaps in rats]. Biull Eksp Biol Med, 1997; 124:229–232.
103.
KiddKR, Dal PonteD, StoneAL, HoyingJB, NagleRB, WilliamsSK. Stimulated endothelial cell adhesion and angiogenesis with laminin-5 modification of expanded polytetrafluoroethylene. Tissue Eng, 2005; 11:1379–1391.
104.
KiddKR, WilliamsSK. Laminin-5-enriched extracellular matrix accelerates angiogenesis and neovascularization in association with ePTFE. J Biomed Mater Res Part A, 2004; 69:294–304.
105.
KibbeyMC, GrantDS, KleinmanHK. Role of the SIKVAV site of laminin in promotion of angiogenesis and tumor growth: an in vivo Matrigel model. J Natl Cancer Inst, 1992; 84:1633–1638.
106.
PonceML, KleinmanHK. Identification of redundant angiogenic sites in laminin alpha1 and gamma1 chains. Exp Cell Res, 2003; 285:189–195.
RousselleP, CarulliS, ChajraH, DayanG, PinD, HerbageB. The syndecan binding sequence KKLRIKSKEK in laminin alpha3 LG4 domain promotes epidermal repair. Eur J Dermatol, 2013 [Epub ahead of print].
109.
ArakiE, MomotaY, TogoT, et al.Clustering of syndecan-4 and integrin beta1 by laminin alpha 3 chain-derived peptide promotes keratinocyte migration. Mol Biol Cell, 2009; 20:3012–3024.
110.
KimJM, ParkWH, MinBM. The PPFLMLLKGSTR motif in globular domain 3 of the human laminin-5 alpha3 chain is crucial for integrin alpha3beta1 binding and cell adhesion. Exp Cell Res, 2005; 304:317–327.
111.
MinSK, LeeSC, HongSD, ChungCP, ParkWH, MinBM. The effect of a laminin-5-derived peptide coated onto chitin microfibers on re-epithelialization in early-stage wound healing. Biomaterials, 2010; 31:4725–4730.
112.
DamodaranG, TiongWH, CollighanR, GriffinM, NavsariaH, PanditA. In vivo effects of tailored laminin-332 alpha3 conjugated scaffolds enhances wound healing: a histomorphometric analysis. J Biomed Mater Res Part A, 2013; 101:2788–2795.
113.
MochizukiM, KadoyaY, WakabayashiY, et al.Laminin-1 peptide-conjugated chitosan membranes as a novel approach for cell engineering. FASEB J, 2003; 17:875–877.
114.
IkemotoS, MochizukiM, YamadaM, et al.Laminin peptide-conjugated chitosan membrane: Application for keratinocyte delivery in wounded skin. J Biomed Mater Res Part A, 2006; 79:716–722.
115.
NakamuraM, MieM, MiharaH, NakamuraM, KobatakeE. Construction of multi-functional extracellular matrix proteins that promote tube formation of endothelial cells. Biomaterials, 2008; 29:2977–2986.
116.
AliS, SaikJE, GouldDJ, DickinsonME, WestJL. Immobilization of cell-adhesive laminin peptides in degradable PEGDA hydrogels influences endothelial cell tubulogenesis. Biores Open Access, 2013; 2:241–249.
117.
FuX, XuM, LiuJ, QiY, LiS, WangH. Regulation of migratory activity of human keratinocytes by topography of multiscale collagen-containing nanofibrous matrices. Biomaterials, 2014; 35:1496–1506.
