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Supramolecular Design of Self-Assembling Nanofibers For Supramolecular design of self-assembling SPECIAL FEATURE nanofibers for cartilage regeneration Ramille N. Shaha,b, Nirav A. Shahc, Marc M. Del Rosario Limd, Caleb Hsieha,b, Gordon Nubere, and Samuel I. Stuppa,b,f,g,1 aInstitute for BioNanotechnology in Medicine, Northwestern University, 303 E. Superior Street 11th floor, Chicago, IL 60611; bDepartment of Materials Science and Engineering, Northwestern University, 2220 Campus Drive, Evanston, IL 60208; cDepartment of Orthopaedic Surgery, Northwestern University, 676 N. Saint Clair, Suite 1350, Chicago, IL 60611; dDepartment of Biomedical Engineering, Northwestern University, 2145 Sheridan Road, Evanston, IL 60208; eNorthwestern Orthopaedic Institute, 680 N. Lakeshore Dr., Suite 1028, Chicago, IL 60611; fDepartment of Chemistry, Northwestern University, 2145 Sheridan Road, Evanston, IL 60208; and gDepartment of Medicine, Northwestern University, 251 East Huron Street, Suite 3-150, Chicago, IL 60611 Edited by Robert Langer, Massachusetts Institute of Technology, Cambridge, MA, and approved December 23, 2009 (received for review June 12, 2009) Molecular and supramolecular design of bioactive biomaterials planted through minimally invasive means that localizes and main- could have a significant impact on regenerative medicine. Ideal tains cells and growth factors within the defect site, promotes stem regenerative therapies should be minimally invasive, and thus cell chondrogenic differentiation, and stimulates biosynthesis. the notion of self-assembling biomaterials programmed to trans- In prior work, we developed self-assembling biomaterials form from injectable liquids to solid bioactive structures in tissue based on a broad class of molecules known as peptide amphi- is highly attractive for clinical translation. We report here on a coas- philes (PAs) that self-assemble from aqueous media into supra- sembly system of peptide amphiphile (PA) molecules designed to molecular nanofibers of high aspect ratio. These molecules, form nanofibers for cartilage regeneration by displaying a high targeted to serve as the components of artificial extracellular ma- density of binding epitopes to transforming growth factor β-1 trices, consists of a peptide segment covalently bonded to a more (TGFβ-1). Growth factor release studies showed that passive hydrophobic segment such as an alkyl tail (9–12). PAs are nor- release of TGFβ-1 was slower from PA gels containing the growth mally charged molecules so that screening ions in the biological factor binding sites. In vitro experiments indicate these materials environment can trigger self-assembly into cylindrical nanofibers, support the survival and promote the chondrogenic differentiation which form by hydrogen bonding among peptide segments into SCIENCES of human mesenchymal stem cells. We also show that these β-sheets and the hydrophobic collapse of their alkyl segments materials can promote regeneration of articular cartilage in a full (13). Furthermore, PAs can have a terminal biosignaling peptide APPLIED BIOLOGICAL thickness chondral defect treated with microfracture in a rabbit domain, which upon self-assembly becomes exposed in very high model with or even without the addition of exogenous growth densities on the surfaces of the nanofibers. At specific pH values factor. These results demonstrate the potential of a completely and PA concentrations, these amphiphilic molecules can assem- synthetic bioactive biomaterial as a therapy to promote cartilage ble into self-supporting gels made up of an interconnected net- regeneration. work of nanofibers (12). Over time, PA gels should biodegrade into amino acids and lipids that can be safely cleared by the body. self-assembling biomaterials ∣ chondral defects ∣ microfracture ∣ We had previously discovered by phage display a peptide se- peptide amphiphiles ∣ transforming growth factor quence (HSNGLPL) with a binding affinity to transforming growth factor β1 (TGF-β1), which is known to be important in amaged articular cartilage in our joints is an important the formation of connective tissues and for other biological Dregenerative medicine target because adults lack the ability functions (14). Prior work has demonstrated that TGF-β1 plays to effectively form cartilage with the architecture and morphol- a significant role in the regulatory network of growth factors that ogy of the native tissue. This can eventually lead to joint pain with maintains articular cartilage in the differentiated phenotype (15) loss of physical function (1–3), a serious health care issue in an and is a critical factor for inducing chondrogenesis in marrow- aging and physically active global population. Full thickness focal derived MSCs (16). Furthermore, in articular cartilage tissue chondral lesions may progress to osteoarthritis that has an engineering TGF-β1 has been shown to increase collagen and estimated economic impact approaching $65 billion in the US proteoglycan production and inhibit matrix breakdown (17). alone when considering healthcare costs, loss of wages, and so- The effectiveness of TGF-β1, however, has also been demon- cietal impact costs (4). With the limited natural healing capability strated to be significantly dependent on the delivery kinetics of articular cartilage, clinical intervention is necessary to prevent and/or simultaneous delivery with other proteins (18, 19). further articular cartilage degradation and early progression of In this study, we designed and evaluated in vivo a unique self- degenerative osteoarthritis. assembling PA molecule, which includes a TGF-binding domain Microfracture is a common clinical procedure used for the re- (Fig. 1A) for specific use in articular cartilage regeneration. This pair of cartilage defects (5). The benefits of microfracture include particular element in artificial matrix design, that is, the binding the fact that it is a single-stage procedure, is relatively simple from of growth factors to components of the extracellular space such as a technical point of view, is cost-effective with low patient morbid- collagens and heparin, have been shown to occur naturally in ity, and involves the patients’ own mesenchymal stem cells (MSCs) biological systems (20, 21). The matrix studied here also con- as a cell source to stimulate cartilage repair. The reparative pro- tained a nonbioactive PA of smaller molecular dimensions cess in microfracture involves a clot of pluripotent MSCs that (Fig. 1B) that coassembles with the TGF-binding molecules. adhere to the subchondral bone. Histological assessment of microfracture in animal (6, 7) and clinical testing (5) have shown Author contributions: R.N.S., N.A.S., and G.N. designed research; R.N.S., N.A.S., M.M.D.R.L., that most lesions form fibrous cartilage with predominant type I and C.H. performed research; R.N.S., N.A.S., M.M.D.R.L., and C.H. analyzed data; and collagen and a limited amount of type II collagen present. Addi- R.N.S., N.A.S., and S.I.S. wrote the paper. tionally, there is a significant drop in clinical outcome scores after The authors declare no conflict of interest. 18 months as well as in patients older than 40 years (8). This sug- This article is a PNAS Direct Submission. gests that there is deficient bioactivity, quantity, quality, and reten- 1To whom correspondence should be addressed at: Northwestern University, Cook Hall, tion of chondrocyte phenotype within the repair tissue. An ideal Room 1127, 2220 Campus Drive, Evanston, IL 60208. E-mail: [email protected]. regenerative medicine solution to augment this current clinical This article contains supporting information online at www.pnas.org/cgi/content/full/ procedure would be a bioactive scaffold capable of being im- 0906501107/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.0906501107 PNAS Early Edition ∣ 1of6 Downloaded by guest on September 25, 2021 microscopy (SEM) revealed cells extended their processes to interact with the surrounding PA nanofiber matrix (Fig. 2B). When grown in chondrogenic media, most MSCs obtained a more rounded phenotype as expected, indicating that the PA gels supported and did not inhibit MSC differentiation. Gene expression analysis for cartilage markers (aggrecan and type II collagen) at 3 and 4 wks showed upregulation of these genes in both filler and TGFBPA that incorporated 100 ng∕mL rhTGF-β1 within the gels (Fig. 2C and Fig. S1). At 3 wks, glyco- saminoglycan (GAG) content in the scaffolds was also assessed and showed significantly higher (p < 0.05) GAG production in the PA gels that contained supplemented growth factor (Fig. 2D), but there was no apparent difference between the filler and TGFBPA at this time point. It is expected that the presence of supplemented TGFβ-1 in both the filler and TGFBPA would result in chondrogenic differentiation of MSCs as long as the therapeutic amount of growth factor is present. At 4 wks, how- Fig. 1. Design of PAs for articular cartilage regeneration. Chemical structure ever, there was a significantly higher aggrecan expression level of (A) TGF-binding PA and (B) nonbioactive filler PA. (C) Illustration of co- for the TGFBPA (10 mol%) compared to the filler PA assembly of the TGF-binding PA and the filler PA showing binding epitopes (p < 0.03). This most likely is the result of prolonged and more exposed on the surface of the nanofiber. (D) ELISA results showing TGFβ-1 localized delivery of the growth factor from the TGFBPA com- release up to 72 hours from filler PA and 10 mol% TGF-binding PA (TGFBPA). 100 ng∕mL of TGFβ-1 were loaded in all gels. Error bars
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