I dropped my AT&T broadband just prior to the Comcast takeover, but once had a similar setup to what you describe (and nslookup worked fine). In the Network preference panel, "DNS Servers" was left blank. At one time i had asked AT&T what the IP address of their DNS servers were, but they wouldn't give me that info. You'd think i had asked for the combination to their corporate vault. I was, however, able to figure it out eventually using nslookup (although i never had the need to use that info).
I don't understand why you're unable to do an nslookup. What do you get when you issue the command from the terminal? Have you tried nslookup while your Mac is connected directly to the cable modem with DHCP set?
I'm not familiar specifically with how Airport works, having never used it myself, but if it's like a typical broadband router, you should be able to tell Airport to talk to the cable using DHCP, and talk to Airport in any way you like (e.g. fixed IP or DHCP). You shouldn't have to enter a DNS server IP in your networking panel as Airport should pass the DNS server info along to your Mac. In other words, i suspect your problem may be in your Airport configuration.
In my current DSL setup, only my router knows the IP of my DNS servers. My Mac doesn't (but it does know the IP of the router). DNS resolves correctly for me (and nslookup works fine).