The molecular basis of autoimmune disease remains enigmatic. Type 1 diabetes (T1D) is an autoimmune disease caused by the T-cell mediated destruction of the insulin-producing beta cells. The HLA genes, HLA-DQ8 and HLA-DQ2, confer the highest risk of developing T1D implicating CD4+ T-cell responses in the pathogenesis of T1D. Efforts to analyze CD4+ T-cell responses in T1D have been hampered by the technical challenges associated with detecting these rare cells in patient blood. To overcome this problem we isolated T cells from the pancreatic islets from organ donors who suffered from T1D. We have focused on the CD4+ T-cells from one donor with the HLA type: HLA DR3-DQ2; DR4-DQ8 that confers very high risk of T1D. We characterized 53 CD4+ T-cell clones and found that 15 (28%) recognized epitopes derived from proinsulin C-peptide. Interestingly, most epitopes clustered in the middle of the C-peptide. Analysis of the clones’ HLA restrictions revealed that all, except one pair of clones with identical TCRs, were restricted by HLA-DQ8 (A1*03:01, B1*03:02). The remaining pair of clones were restricted by an HLA-DQ8 transdimer (DQA1*05:01, DQB1*03:02). To investigate responses to these epitopes in patients’ blood we performed CFSE-based proliferation assays. Two of eight children with recent onset T1D, but none of five HLA-matched controls had CD4+ T-cell responses to these epitopes. This is the first functional analysis of human islet-infiltrating CD4+ T cells. Our work confirms CD4+ T-cells’ role in in the pathogenesis of human T1D and links the HLA-DQ8 responses to proinsulin.